Citation: Jerry R. Miller, John P. Gannon, Kyle Corcoran. Concentrations, mobility, and potential ecological risks of selected metals within compost amended, reclaimed coal mine soils, tropical South Sumatra, Indonesia[J]. AIMS Environmental Science, 2019, 6(4): 298-325. doi: 10.3934/environsci.2019.4.298
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Bacterial adherence factors, also known as adhesins, are proteins on the cell surface that form and maintain physical interactions with host cells and tissues. They are important in both health and disease as they are needed by pathogens for infection and by commensal or “good” bacteria to maintain a symbiotic relationship with the host. Surprisingly, several dozen of these proteins were previously identified as ubiquitous intracellular enzymes that have a canonical function in essential cellular processes and are sometimes referred to as “housekeeping enzymes” [1,2,3,4,5]. The first intracellular/surface moonlighting protein (ISMP) to be identified was an enzyme in glycolysis, glyceraldehyde 3-phosphate dehydrogenase (GAPDH), which has a second role on the surface of pathogenic streptococci [6]. Other intracellular/surface moonlighting proteins include other metabolic enzymes that are also widespread in evolution and function in glycolysis, the citric acid cycle, or DNA and protein metabolism, for example, phosphoglycerate kinase and enolase. Intracellular chaperones (Hsp60/GroEL, Hsp70/DnaK), and protein synthesis elongation factors (EF-Tu, EF-G) have also been found to serve as adhesins in bacteria (Table 1).
In general, moonlighting proteins comprise a subset of multifunctional proteins that perform two or more distinct and physiologically relevant biochemical or biophysical functions that are not due to gene fusions, multiple RNA splice variants, or pleiotropic effects [1]. The MoonProt Database includes information about hundreds of moonlighting proteins for which biochemical or biophysical evidence supports the presence of at least two biochemical functions in one polypeptide chain [7]. Of these, over 30 types of proteins have one function inside the cell and another function as an adhesin on the cell surface. Some are found to moonlight on the surface of multiple species, so there are over 100 ISMPs. The bacterial ISMPs (Table 1) are found in typical Gram-positive and Gram-negative species, as well as mycobacteria, spirochetes, and mycoplasma.
An ISMP can have different extracellular functions in different species. Enolase converts the reversible conversion of 2-phosphoglycerate to phosphoenolpyruvate in the cytoplasm in glycolysis and gluconeogenesis and has been found to have many moonlighting functions in addition to being an adhesin on the bacterial cell surface. As a bacterial adhesin, enolase binds host proteins in the extracellular matrix, mucin, and other proteins and plays an important role in infection of mammalian and avian hosts [8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24] (Figure 1). Some ISMPs also have third (or more) functions as secreted soluble proteins, in many cases with roles in modulation of the immune system [2,3].
In pathogenic bacteria the extracellular function often plays a key role in infection or virulence [2,3]. ISMPs have been found to be involved in aiding the bacteria to bind directly to host cells, including fructose-1,6-bisphosphate aldolase from Neisseria meningitidis [25] and Streptococcus pneumoniae [26] and the Hsp60 chaperone from Clostridium difficile [27], Helicobacter pylori [28], Chlamydia pneumoniae [29], Legionella pneumophila [30] and several other species. In some cases a specific receptor on the host cell surface has been identified. Listeria monocytogenes alcohol acetaldehyde dehydrogenase binds to Hsp60 (another moonlighting protein) on the surface of several human cell lines [31,32]. Streptococcus pyogenes GAPDH binds to the uPAR/CD87 receptor [33]. Streptococcus pneumoniae fructose 1,6-bisphosphate aldolase binds to the flamingo cadherin receptor (FCR) [26]. Haemophilus ducreyi Hsp60 binds to membrane glycosphingolipids [34,35].
Other ISMPs bind to extracellular matrix or secreted mucins in the mucosal layer of the intestines and airway. Mycoplasma pneumoniae EF-Tu and pyruvate dehydrogenase, Mycobacterium tuberculosis malate synthase, and Streptococcus mutans autolysin AltA, Staphylococcus caprae autolysin AltC, and Staphylococcus aureus autolysin Aaa bind to one or more of the extracellular matrix components fibronectin, laminin, and/or collagen [36,37,38,39,40]. Mycoplasma genitalium GAPDH, Salmonella typhimurium Hsp60, and Streptococcus gordonii enolase, EF-Tu, and the beta subunit of the DNA-directed RNA polymerase bind mucin [18,41,42]. Other examples are given in Table 1.
Figure 1. Intracellular enzymes and chaperones can function as adhesins on the bacterial cell surface. An ISMP can function as an enzyme inside of the cell and an adhesin when located on the cell surface. Enolase is found in the cytoplasm in almost all species where it converts 2-phosphoglycerate to phosphoenolpyruvate as the ninth step of glycolysis. In many species of bacteria, it is also found on the cell surface where it can bind to the host's extracellular matrix or airway mucins. For pathogenic bacteria, this attachment can be important for invading host tissues and promoting infection. In most cases, how the intracellular enzyme is transported outside the cell and how it becomes attached to the cell surface are not known (curved arrow). There might be a receptor for the protein on the bacterial cell surface (hexagon), but the nature of the surface attachment is known for only a few ISMPs.The ability of many pathogenic bacteria to use surface proteins to bind to the soluble host protein plasminogen also assists in invasion of host tissues [11,12,13,14,43,44]. Plasminogen is a precursor to plasmin, which is a broad-spectrum serine protease present in blood that helps break down fibrin clots [45]. When an invading pathogen uses a receptor on its surface to bind plasminogen from the host, the plasminogen can be converted to plasmin, the active form of the protease, by using an endogenous protease or subverting the host's tissue-type plasminogen (tPA) activators and urokinase-type plasminogen activators [46]. The active plasmin that is then attached to the surface of the invading organism can be used as a general protease to degrade host extracellular matrix and basement membrane, thereby facilitating migration through tissues. In the case of Mycoplasma hyopenumoniae, a swine-specific pathogen with a reduced genome that lacks genes for building amino acids, having an active protease on the surface enables cleavage of a variety of host proteins to produce peptides and amino acids that can be taken up by the bacterium as nutrients [47,48]. Other ISMPs also aid in infection and virulence by serving as receptors on the bacterial cell surface to acquire nutrients from the host. Staphylococcal GAPDH serves as a transferrin binding protein to acquire iron from the host [49].
The use of moonlighting proteins in adherence to host cells and tissues is not seen only in pathogenic species. Bacterial species that are sometimes referred to as “good” bacteria or probiotics, in other words nonpathogenic symbionts that help promote health and well-being, use ISMP in commensal interactions with host species, especially in the intestines. Lactobacillus plantarum GAPDH and enolase were shown to aid the bacterium in binding to mammalian cells and could play a role for this probiotic species to bind to the lining of the gut [23,50]. Lactobacillus johnsonii EF-Tu and Hsp60 also bind to human cells and to mucin [51,52]. Lactobacillus acidophilus GAPDH also binds mucin [53].
ISMPs may also assist in symbiotic relationships with other species, including a symbiotic relationship between lactic acid bacteria and yeast. The bacteria break down starch and other carbohydrates to produce lactic acid that is used by the yeast. In return they receive nutrients made by the yeast. This symbiotic relationship is found in several kinds of fermented foods like kefir, a drink made from cow's milk. Lactococcus lactis GAPDH, pyruvate kinase, Hsp60/GroEL, DnaK/Hsp70, and 6-phosphofructokinase have been shown to bind to invertase on the surface of the yeast Saccharomyces cerevisiae to help maintain this inter-species symbiotic interaction [54].
One of the benefits of probiotic bacteria has been suggested to be that they compete with pathogens for binding sites or nonspecific binding to the surface of epithelial cells lining the gut. Several moonlighting proteins were found to aid Lactobacillus species in competing with pathogenic species for binding to epithelial cell lines in vitro. Some of the same ISMPs may be involved in the competition of pathogenic and commensal bacteria for binding to epithelial cells. Several of the moonlighting proteins have been found to perform the same combination of enzyme and adhesion functions in both pathogenic and commensal bacteria, for example, enolases from Lactobacillus, Staphylococcus, Streptococcus and several other species bind human plasminogen [14].
The adhesion functions of the ISMPs in Table 1 were mainly found through experiments to identify proteins that bind to a specific molecular target, such as collagen, fibronectin, or other extracellular matrix proteins or through studies of proteins involved in binding to a specific target cell type. In recent years, many more intracellular proteins have been found to have a second location on the cell surface through surface proteomics, or “surfomics”, studies that aimed to identify all the proteins on a cell surface [55]. Surface proteomics studies employ variations of three types of experimental approaches to identify cell surface proteins. The main difference in the methods is in how the candidate proteins are isolated: through fractionating the cells to isolate components of the cell membrane and/or cell wall, surface “shaving” or using proteases to digest proteins on the cell surface without damaging the cell membrane, or labeling proteins on the surface with biotin or O18 before disrupting the cells and isolating the proteins. In each case the surface proteins are then identified using mass spectrometry. Although these methods might incorrectly identify some strictly intracellular proteins as being part of the cell surface proteome due to experimental artifacts inherent in the challenges of cell fractionation, and even some intracellular proteins that are correctly found to have a second location on the cell surface might have a different function other than as adhesins, at least some of the known intracellular/surface adhesins were correctly found to be localized to the cell surface, and it is possible that some of the additional cytoplasmic proteins found in these studies are also moonlighting as adhesins. Additional experiments are needed to determine if the intracellular proteins identified as being on the cell surface through proteomics methods are indeed involved in bacterial adhesion and were not found on the surface because they have another role on the surface or perhaps they were artifacts of the experimental methods.
It might at first seem unlikely that so many intracellular chaperones and enzymes required for central metabolism evolved to function also as cell surface binding proteins. Acquiring the new function required (1) evolution of a new protein-protein interaction site as well as (2) mechanisms for secretion and cell surface attachment, all while maintaining the first function of the protein. Satisfying the first requirement can be surprisingly simple. In general, most of the amino acid residues on a protein's surface are not directly connected to the protein's main function and are therefore not under significant selective pressure during evolution. In fact, surface amino acids vary a great deal even among close homologues. Having just a small number of these surface residues in a correct three-dimensional arrangement can be sufficient for formation of a novel protein-protein interaction site. In fact, Ehinger and coworkers showed that a nine amino acid sequence on the surface of enolase was sufficient for its interaction with plasminogen [56]. In general, for an average protein comprised of 300 or 400 amino acids, there is ample space and material for development of a new protein-protein binding site. In addition, most of these proteins are essential housekeeping proteins that first evolved billions of years ago and are expressed in many species and cell types, providing both the time and variety of cellular conditions for evolution of the protein surface to include a new binding function.
A more difficult question is how most of the ISMPs are secreted and become attached to the cell surface. The ISMPs do not contain a signal sequence or the twin arginine motif found in most proteins secreted by the canonical Sec or TAT secretion systems, respectively. For these reasons, the ISMPs are sometimes referred to as anchorless surface proteins or surface-associated housekeeping enzymes and are said to be secreted through non-classical, noncanonical, or unconventional secretion pathways. It is not clear if any of the known non-canonical secretion systems are involved in the secretion of ICMS, but most still require a kind of secretion signal, and they tend to be involved in the secretion of a few specific proteins [57].
Although it has been suggested that these intracellular proteins could become released from dead or damaged cells, several lines of evidence support the idea that at least some of them do require a secretion system [58,59]. First, the ISMPs are not the most abundant proteins in the cell, and those proteins that are most abundant are not often found on the cell surface. Second, a large portion of the pool of each protein type remains inside the cell while only some of the pool of the protein is partitioned to the cell surface. Why only part of the cytoplasmic pool of these specific proteins become targeted to the cell surface is not known.
For some individual proteins, there is additional evidence that a secretion system is probably involved. Yang and coworkers concluded that the release of GroEL, DnaK, enolase, pyruvate dehydrogenase subunits PdhB and PdhD, and superoxide dismutase SodA, by Bacillus subtilis is not due to gross cell lysis based on observing a constant cell density, no change in secretion in the presence of chloramphenicol, constant cell viability count, negligible amounts of two highly expressed cytoplasmic proteins EF-Tu and SecA in the culture medium, and the lack of effect of deleting lytC and lytD autolysins on the amount of the proteins in the media [60]. They also showed that these proteins were not released into the medium by membrane vesicles and there was no N-terminal cleavage (which might have suggested the presence of a signal sequence). Also, a mutant form of enolase with a hydrophobic helix replaced with a more neutral helix was retained in the cell when the wild type protein was found in the media, which also supports the model that it is not due to cell lysis. They followed up by showing that in Bacillus subtilis enolase, the internal hydrophobic helical domain was essential but not sufficient for export of enolase [61], although a larger portion of the N-terminal domain (residues 1-140) was sufficient for export of GFP in B subtilis and E coli. Boel and colleagues found that Lys341 of E. coli, Enterococcus faecalis, and Bacillus subtilis enolase becomes spontaneously modified with the substrate 2-phosphoglycerate (2PG), and this post-translational modification is required for export form the cell [62]. Substitution of Lys341 with other amino acids (Ala, Arg, Glu, Gln) prevented modification and secretion even though the Lys341Glu mutant enzyme was enzymatically active, showing that enzyme activity was not sufficient for secretion (and also that secretion was not due to cell leakage, because a single amino acid change can cause a decrease in secretion).
Secretion of some ISMPs may involve an as yet unknown secretion pathway, or their secretion might utilize an alternative version of one or more of the known secretion systems. If the latter is true, there are several possibilities, which are not mutually exclusive: One or more of the known secretion systems could be leaky. Post translational modifications (PTMs), possibly transient PTMs, can render some subset of the ISMP to be passable substrates. Alternative versions of the secretion systems might exist that require additional proteins such as a chaperone that have not yet been identified. An alternative system's secretion could be in competition with folding/unfolding or only rare conformations of an ISMP might be competent for secretion. It's possible that some combination of these factors could result in an inefficient secretion process, or that the alternative version requires induction of the expression of an unknown protein component of a known secretion system or an enzyme involved in adding PTMs. A search for shared characteristics might suggest what protein features singled out these intracellular proteins for adoption to play a second role on the cell surface, but a study of 98 ISMPs found that they share physical characteristics typical of intracellular proteins [63]. A couple studies have identified peptides on the cell surface that are the results of proteolytic cleavage of intracellular proteins, including EF-Tu [64,65], and the authors suggested that cleavage might yield peptides that are better at binding to some host proteins than the intact ISMPs. Because intact versions of these proteins are also found on the cell surface, the proteolytic cleavage is likely to take place after transport across the membrane and not as part of the secretion mechanism.
After the intracellular proteins are transported to the extracellular milieu, they become anchored to the surface of the bacterial cells, but in most cases, the mechanism for cell surface anchoring is also not known. For surface proteins in general, known anchoring mechanisms involve an N-terminal signal sequence for secretion and/or a C-terminal sorting motif, such as the LPXTG motif that is recognized by sortase A, for anchoring to the peptidoglycan network on the cell surface [66]. A smaller number of surface proteins have been found to be targeted to the cell surface due to the presence of additional motifs [67,68,69], including the GW repeat, the choline binding motif, and the LysM domain, but these are not found in the majority of the ISMPs in Table 1. Studies with purified proteins have shown that some intracellular/surface moonlighting proteins can adhere to the cell surface by re-association in both Gram-positive and Gram-negative bacteria, so it is possible that some of the ISMPs are secreted and then re-associate with the cell surface of after secretion. An increase in extracellular pH has been shown to cause some Lactobacillus crispatus ISMPs to be released from the cell surface [70]. Some ISMPs may also be released from the surface during cell-wall renewal that occurs during exponential growth phase [71]. In most cases it is not known to which components of the cell surface—proteins, lipids, etc.—the proteins bind, but it was shown recently that extracellular enolase is bound to a rhamnose residue in cell membrane of mycoplasma [72], and enolase and GAPDH bind covalently to lipotectoic acid on Lactobacillus crispatus [73].
With the increasing problem of antibiotic resistance [74,75], new methods for inhibiting bacterial infections and virulence are needed, and studies of ISMPs might provide new targets for the development of novel therapeutics. But it's not the moonlighting proteins themselves that might be the best targets. The catalytic mechanisms of most of these ISMP are conserved between bacteria and their human hosts, which makes sense because they play key roles in central metabolic pathways such as glycolysis. Instead of targeting the ISMPs, elucidating how these proteins are targeted to the bacterial cell surface might identify processes and proteins that are involved in the novel secretion systems (or new versions of known secretion systems) or surface attachment mechanisms and that could serve as novel targets for developing new strategies for controlling infection.
Learning how pathogenic and commensal bacteria adhere to host cells and tissues could also lead to better understanding of how these species colonize host tissues and compete with each other. This information can be important in treatment of diseases that involve an imbalance of pathogenic and probiotic bacterial species, for example ulcerative colitis and Crohn's disease [76], which are autoimmune diseases of the gut that affect over a million people in the US alone [77]. Understanding bacterial adhesion could potentially lead to information about how probiotic species could be used to displace pathogens and improve the balance of bacterial species.
| Protein | Species | UniProt ID | Extracellular function | References |
| 6-phosphofructokinase | Lactococcus lactis | P0DOB5 | yeast invertase | [54] |
| Streptococcus oralis | E6KMA1 | plasminogen | [78] | |
| Aaa autolysin | Staphylococcus aureus | Q2YVT4 | fibronectin | [37] |
| Aae autolysin | Staphylococcus epidermis | Q8CPQ1 | fibrinogen, fibronectin, vitronectin | [79] |
| Aspartase | Haemophilus influenzae | P44324 | plasminogen | [80] |
| Atla autolysin | Streptococcus mutans | U3SW74 | fibronectin | [39] |
| AtlC autolysin | Staphylococcus caprae | Q9AIS0 | fibronectin | [40] |
| Bile salt hydrolase | Bifidobacterium lactis | Q9KK62 | plasminogen | [81] |
| C5a peptidase | Streptococcus agalactiae | Q8E4T9 | fibronectin | [82] |
| DNA-directed RNA polymerase beta subunit | Streptococcus gordonii | A0EKJ1 | Muc7 | [18] |
| DnaK | Bifidobacterium | Q8G6W1 | plasminogen | [81] |
| Lactococcus lactis | P0A3J0 | yeast invertase | [54] | |
| Mycobacterium tuberculosis | A0A0H3L5C8 | plasminogen | [75] | |
| Neisseria meningitidis | A9M296 | plasminogen | [20] | |
| EF-Tu | Lactobacillus johnsonii | Q74JU6 | cells, mucins | [51] |
| Mycoplasma pneumoniae | P23568 | fibronectin, epithelial cells, plasminogen, heparin, fetuin, actin, fibrinogen, vitronectin, laminin | [36,64] | |
| Pseudonomas aeruginosa | P09591 | plasminogen | [43] | |
| Streptococcus gordonii | A8AWA0 | Muc7 | [18] | |
| Elongation factor G | Streptococcus gordonii | A8AUR6 | Muc7 | [18] |
| Endopeptidase O | Streptococcus pneumoniae | Q8DNW9 | plasminogen, fibronectin | [83] |
| Enolase | Aeromonas hydrophila | Q8GE63 | plasminogen | [22] |
| Bacillus anthracis | D8H2L1 | plasminogen, laminin | [8] | |
| Bifidobacterium lactis | B7GTK2 | plasminogen | [11] | |
| Borrelia burgdorferi | B7J1R2 | plasminogen | [16] | |
| Lactobacillus crispatus | Q5K117 | plasminogen, laminin | [14] | |
| Lactobacillus johnsonii | Q74K78 | plasminogen, laminin | [14] | |
| Lactobacillus plantarum | Q88YH3 | fibronectin | [23] | |
| Leishmania mexicana | Q3HL75 | plasminogen | [13] | |
| Mycoplasma fermentans | C4XEI3 | plasminogen | [24] | |
| Mycoplasma suis | F0QRW4 | red blood cells | [84] | |
| Mycoplasma synoviae | Q4A740 | plasminogen, fibronectin | [9] | |
| Neisseria meningitidis | E0N8L2 | plasminogen | [20] | |
| Staphylococcus aureus | Q6GB54 | plasminogen, laminin | [14,21] | |
| Streptococcus canis | I7WI49 | plasminogen | [17] | |
| Streptococcus gordonii | A8AY46 | Muc7 | [18] | |
| Streptococcus mutans | Q8DTS9 | plasminogen | [12] | |
| Streptococcus oralis | A0A1F1EC06 | plasminogen | [19] | |
| Streptococcus pneumoniae | Q97QS2 | plasminogen | [14] | |
| Streptococcus pyogenes | Q1JML5 | plasminogen | [14] | |
| Streptococcus suis | A4W2T1 | fibronectin, plasminogen | [15] | |
| Fructose 1,6-bisphosphate aldolase | Neisseria meningitidis | F0N9L0 | cells | [25] |
| GAPDH | Bacillus anthracis | Q81X74 | plasminogen | [85] |
| Lactobacillus acidophilus | Q5FL51 | mucin | [53] | |
| Lactobacillus plantarum | F9UM10 | mucin, Caco-2 cells | [50] | |
| Lactococcus lactis | P52987 | yeast invertase | [54] | |
| Mycoplasma genitalium | P47543 | mucin | [41] | |
| Staphylococcus aureus | Q6GIL8 | transferrin | [49] | |
| Streptococcus agalactiae | Q9ALW2 | plasminogen | [86] | |
| Streptococcus oralis | A0A0F2E7M6 | plasminogen | [78] | |
| Streptococcus pneumoniae | A0A0H2US80 | plasminogen | [87] | |
| Streptococcus pyogenes | P68777 | uPAR/CD87 receptor on human cells, plasminogen | [33,88] | |
| Streptococcus suis | Q3Y454 | plasminogen | [89] | |
| Glucose 6-phosphate isomerase | Lactobacillus crispatus | K1MKZ7 | laminin, collagen | [90] |
| Glutamine synthetase | Lactobacillus crispatus | D5GYN9 | fibronectin, laminin, collagen I, plasminogen | [90] |
| Mycobacterium tuberculosis | A0A0H3LHU4 | plasminogen, fibronectin | [91] | |
| Bifidobacterium lactis | C2GUH0 | plasminogen | [81] | |
| Hsp60 | Chlamydiae pneumoniae | P31681 | adhesin | [29] |
| Lactococcus lactis | P37282 | yeast invertase | [54] | |
| Legionella pneumophila | Q5X762 | adhesin | [30] | |
| Clostridium difficile | Q9KKF0 | adhesin | [27] | |
| Haemophilus ducreyi | P31294 | glycosphinngolipids | [34,35] | |
| Helicobacter pylori | Q8RNU2 | adhesin | [28] | |
| Lactobacillus johnsonii | F7SCR2 | adhesin | [52] | |
| Listeria | Q8KP52 | adhesin | [32] | |
| Salmonella typhimurium | P0A1D3 | mucus | [42] | |
| Hsp65/Cpn60.2/GroEL2 | Mycobacterium tuberculosis | A0A0H3LCC3 | CD43 on macrophage surface | [92] |
| Leucyl aminopeptidase | Mycoplasma hyopneumoniae | Q4A9M4 | heparin | [93] |
| Malate synthase | Mycobacterium tuberculosis | P9WK17 | fibronectin, laminin, epithelial cells | [38] |
| Glutamyl aminopeptidase | Mycoplasma hyopneumoniae | Q4AAK4 | plasminogen, heparin | [47] |
| Leucyl aminopeptidase | Mycoplasma hyopneumoniae | Q4A9M4 | plasminogen, heparin, DNA | [48] |
| Ornithine carbamoyltransferase | Staphylococcus epidermidis | P0C0N1 | fibronectin | [94] |
| Peroxiredoxin | Neisseria meningitidis | A0A125WDU3 | plasminogen | [20] |
| Streptococcus agalactiae | E7S2A7 | heme | [95] | |
| Phosphoglycerate kinase | Streptococcus oralis | A0A0G7HBY7 | plasminogen | [77] |
| Streptococcus agalactiae | Q8DXT0 | plasminogen, actin | [83,96] | |
| Streptococcus pneumoniae | Q8DQX8 | plasminogen | [97] | |
| Phosphoglycerate mutase | Bifidobacterium lactis | P59159 | plasminogen | [81] |
| Streptococcus oralis | E6IYJ0 | plasminogen | [78] | |
| Pyruvate dehydrogenase | Mycoplasma pneumoniae | P75391 | fibrinogen | [36] |
| Pyruvate kinase | Lactococcus lactis | Q07637 | yeast invertase | [54] |
| Superoxide dismutase | Mycobacterium avium | P53647 | adhesin | [98] |
| Triose phosphate isomerase | Streptococcus oralis | E6J203 | plasminogen | [78] |
DownLoad: CSVThe large number of ISMPs, the variety of bacterial species, and the different host proteins targeted suggests that this phenomenon of intracellular housekeeping proteins moonlighting as adhesins on the bacterial cell surface is widespread. There is still a great deal to learn about these proteins, especially how these intracellular proteins are secreted and attached to the bacterial cell surface. Studies of ISMP that serve as adhesins could help in identifying novel targets for development of therapeutics because their mechanisms of secretion and membrane attachment are likely to involve new proteins and cellular processes.
The author declares no conflict of interest in this paper.
| [1] | Syarif A (2014) Characterization of geochemical waste rock, and mitigation of acid mine drainage at coal mining Bukit Asam. Sriwij Int Semin Energy. Environ Sci Technol 1: 149–152. |
| [2] |
Haigh MJ (1980) Slope retreat and gullying on revegetated surface mine dumps, waun hoscyn, gwent. Earth Surf Process 5: 77–79. doi: 10.1002/esp.3760050108
|
| [3] | Kilmartin MP (1994) Runoff Generation and Soils on Reclaimed Land, Blaenant, South Wales. Ph.D., Oxford Brookes University. |
| [4] | Sheoran V, Sheoran A, Poonia P (2010) Soil Reclamation of Abandoned Mine Land by Revegetation: A Review. Int J Soil Sediment Water 3, article 13. Available from https://scholarworks.umass.edu/intljssw/vol3/iss2/13. |
| [5] |
Macdonald SE, Landhäusser SM, Skousen J, et al. (2015) Forest restoration following surface mining disturbance: challenges and solutions. New For 46: 703–732. doi: 10.1007/s11056-015-9506-4
|
| [6] | Haigh M, Kilmartin MP (2015) Reclaimed Opencast Coal Lands in Southeast Wales: Impacts on Water Quality. Amsterdam, IOC Press. |
| [7] |
Hudson-Edwards KA, Jamieson HE, Lottermoser BG (2011) Mine wastes: past, present, future. Elements 7: 375–380. doi: 10.2113/gselements.7.6.375
|
| [8] | Geidel G, Caruccio FT (2000) Geochemical factors affecting coal mine drainage quality. Reclam Drastic Disturb Lands 125–129. |
| [9] |
RoyChowdhury A, Sarkar D, Datta R (2015) Remediation of Acid Mine Drainage-Impacted Water. Curr Pollut Rep 1: 131–141. doi: 10.1007/s40726-015-0011-3
|
| [10] | Kundu NK, Ghose MK (1997) Soil profile characteristic in Rajmahal Coalfield area. Indian J Soil Water Conserv 25: 28–32. |
| [11] |
Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50: 775–780. doi: 10.1016/S0045-6535(02)00232-1
|
| [12] |
Maiti SK (2007) Bioreclamation of coalmine overburden dumps-with special emphasis on micronutrients and heavy metals accumulation in tree species. Environ Monit Assess 125: 111–122. doi: 10.1007/s10661-006-9244-3
|
| [13] |
Massey HF, Barnhisel RI (1972) Copper, nickel, and zinc released from acid coal mine spoil materials of eastern Kentucky. Soil Sci 113: 207. doi: 10.1097/00010694-197203000-00011
|
| [14] | Allen HE, Huang C-P, Bailey GW, Bowers AR (1994) Metal Speciation and Contamination of Soil. CRC Press. |
| [15] |
Dang Z, Liu C, Haigh MJ (2002) Mobility of heavy metals associated with the natural weathering of coal mine spoils. Environ Pollut 118: 419–426. doi: 10.1016/S0269-7491(01)00285-8
|
| [16] |
Maiti SK, Rana V (2017) Assessment of Heavy Metals Contamination in Reclaimed Mine Soil and their Accumulation and Distribution in Eucalyptus Hybrid. Bull Environ Contam Toxicol 98: 97–104. doi: 10.1007/s00128-016-1966-5
|
| [17] | Pietrzykowski M, Socha J, van Doorn NS (2014) Linking heavy metal bioavailability (Cd, Cu, Zn and Pb) in Scots pine needles to soil properties in reclaimed mine areas. Sci Total Environ 470: 501–510. |
| [18] |
Chiou CT, Porter PE, Schmedding DW (1983) Partition equilibriums of nonionic organic compounds between soil organic matter and water. Environ Sci Technol 17: 227–231. doi: 10.1021/es00110a009
|
| [19] |
Chen Y, Yuan L, Xu C (2017) Accumulation behavior of toxic elements in the soil and plant from Xinzhuangzi reclaimed mining areas, China. Environ Earth Sci 76: 226. doi: 10.1007/s12665-017-6535-7
|
| [20] |
Holl KD (2002) Long-term vegetation recovery on reclaimed coal surface mines in the eastern USA. J Appl Ecol 39: 960–970. doi: 10.1046/j.1365-2664.2002.00767.x
|
| [21] | Cravotta CA (2010) Abandoned Mine Drainage in the Swatara Creek Basin, Southern Anthracite Coalfield, Pennsylvania, USA: 2. Performance of Treatment Systems. Mine Water Environ 29: 200–216. |
| [22] |
Walter CA, Nelson D, Earle JI (2012) Assessment of Stream Restoration: Sources of Variation in Macroinvertebrate Recovery throughout an 11-Year Study of Coal Mine Drainage Treatment. Restor Ecol 20: 431–440. doi: 10.1111/j.1526-100X.2011.00845.x
|
| [23] |
Mays PA, Edwards GS (2001) Comparison of heavy metal accumulation in a natural wetland and constructed wetlands receiving acid mine drainage. Ecol Eng 16: 487–500. doi: 10.1016/S0925-8574(00)00112-9
|
| [24] |
Ye ZH, Whiting SN, Qian JH, et al. (2001) Trace Element Removal from Coal Ash Leachate by a 10-Year-Old Constructed Wetland. J Environ Qual 30: 1710–1719. doi: 10.2134/jeq2001.3051710x
|
| [25] | Kuter N (2013) Reclamation of Degraded Landscapes due to Opencast Mining. Adv Landsc Archit. Adv Landscape Archit 33: 823–858. |
| [26] |
Lone MI, He Z, Stoffella PJ, Yang X (2008) Phytoremediation of heavy metal polluted soils and water: Progresses and perspectives. J Zhejiang Univ Sci B 9: 210–220. doi: 10.1631/jzus.B0710633
|
| [27] |
Kavamura VN, Esposito E (2010) Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol Adv 28: 61–69. doi: 10.1016/j.biotechadv.2009.09.002
|
| [28] | Singh AN, Raghubansh AS, Singh JS (2002) Plantations as a tool for mine spoil restoration. Curr Sci 82: 1436–1441. |
| [29] | World Coal Association (2015). World Coal Association, Coal Facts 2014. Available from https://www.worldcoal.org/coal-facts-2014. |
| [30] | Rosyid FA, Adachi T (2016) Forecasting on Indonesian Coal Production and Future Extraction Cost: A Tool for Formulating Policy on Coal Marketing. Nat Resour 07: 677–696. |
| [31] | Greenpeace (2014) Coal mines polluting South Kalimantan's water. Green Peace Southeast Asia. |
| [32] | PT Bukit Asam | Environment. Available from http://www.ptba.co.id/en/environment#post-mining. |
| [33] | Minister of Forestry I (2011) Forest Reclamation Guidelines Indonesia Ministry of Forestry.The Republic of Indonesia. Available from: http://extwprlegs1.fao.org/docs/pdf/ins107031.pdf. |
| [34] | Hermawan B, KSH, Sukisno S (2012) A model of post-mined land reclamation for poberty alleviation: a case study in coal mining of south Sumatra. In: 3 rd International Seminar, Regional Network on Poverty Eradication In Conjunction With UNESCO International Days, Years, Decades, 2012 University of Bengkulu, Indonesia, October 15 th – 17 th 2012. Universitas Bengkulu. |
| [35] |
Soumaré M, Tack FMG, Verloo MG (2003) Characterisation of Malian and Belgian solid waste composts with respect to fertility and suitability for land application. Waste Manag 23: 517–522. doi: 10.1016/S0956-053X(03)00067-9
|
| [36] | He X-T, Logan TJ, Traina SJ (1995) Physical and Chemical Characteristics of Selected U.S. Municipal Solid Waste Composts. J Environ Qual 24: 543–552. |
| [37] |
Jordão CP, Nascentes CC, Cecon PR, et al. (2006) Heavy Metal Availability in Soil Amended with Composted Urban Solid Wastes. Environ Monit Assess 112: 309–326. doi: 10.1007/s10661-006-1072-y
|
| [38] |
Smith SR (2009) A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge. Environ Int 35: 142–156. doi: 10.1016/j.envint.2008.06.009
|
| [39] |
Moon J-W, Goltz MN, Ahn K-H, Park J-W (2003) Dissolved organic matter effects on the performance of a barrier to polycyclic aromatic hydrocarbon transport by groundwater. J Contam Hydrol 60: 307–326. doi: 10.1016/S0169-7722(02)00084-0
|
| [40] |
Moeckel C, Monteith DT, Llewellyn NR, et al. (2014) Relationship between the Concentrations of Dissolved Organic Matter and Polycyclic Aromatic Hydrocarbons in a Typical U.K. Upland Stream. Environ Sci Technol 48: 130–138. doi: 10.1021/es403707q
|
| [41] |
Beesley L, Inneh OS, Norton GJ, et al. (2014) Assessing the influence of compost and biochar amendments on the mobility and toxicity of metals and arsenic in a naturally contaminated mine soil. Environ Pollut 186: 195–202. doi: 10.1016/j.envpol.2013.11.026
|
| [42] | Gautama R (1994) Acid Water Problem in Bukit Asam Coal Mine, South Sumatra, Indonesia. International Mine Water Association, 1994 Proceedings. |
| [43] |
Amijaya H, Littke R (2006) Properties of thermally metamorphosed coal from Tanjung Enim Area, South Sumatra Basin, Indonesia with special reference to the coalification path of macerals. Int J Coal Geol 66: 271–295. doi: 10.1016/j.coal.2005.07.008
|
| [44] | Coster GLD (1974) The Geology of the Central and South Sumatra Basins. 77–110. |
| [45] | Juniarto, A (2018) Pemanfaatan Limbah Organik untuk Produksi Kompos Skala Industri dalam Mendukung Reklamasi Lahan Bekas Tambang. M.S. Thesis, Bogor Agricultural University, Indonesia. Available from http://repository.ipb.ac.id/xmlui/handle/123456789/92688. |
| [46] | Dowdy RH, Volk VV (1983) Movement of Heavy Metals in Soils 1. Chem Mobil React Soil Syst sssaspecialpub l: 229–240. |
| [47] | Sherene T (2010) Mobility and transport of heavy metals in polluted soil environment. Biol Forum 2: 112–121. |
| [48] |
Villarroel LF, Miller JR, Lechler PJ et al. (2006) Lead, zinc, and antimony contamination of the Rio Chilco-Rio Tupiza drainage system, Southern Bolivia. Environ Geol 51: 283–299. doi: 10.1007/s00254-006-0326-x
|
| [49] | Moore O (2016) What Factors Control the Chemistry of the Bukit Asam Coalmines of the South Sumatra Basin. Masters Thesis, Aberystwyth University. |
| [50] | Sloss L (2013) Coal Mine Site Reclamation. IEA Clean Coal Center, Report CCC/216. |
| [51] |
Zamani AA, Yaftian MR, Parizanganeh A (2012) Multivariate statistical assessment of heavy metal pollution sources of groundwater around a lead and zinc plant. Iran J Environ Health Sci Eng 9: 29. doi: 10.1186/1735-2746-9-29
|
| [52] |
Horowitz AJ, Elrick KA (1987) The relation of stream sediment surface area, grain size and composition to trace element chemistry. Appl Geochem 2: 437–451. doi: 10.1016/0883-2927(87)90027-8
|
| [53] | Horowitz AJ, Horowitz AJ (1991) Primer on Sediment-trace Element Chemistry. Lewis Publishers. |
| [54] |
Matys Grygar T, Popelka J (2016) Revisiting geochemical methods of distinguishing natural concentrations and pollution by risk elements in fluvial sediments. J Geochem Explor 170: 39–57. doi: 10.1016/j.gexplo.2016.08.003
|
| [55] |
Ho HH, Swennen R, Cappuyns V, et al. (2012) Necessity of normalization to aluminum to assess the contamination by heavy metals and arsenic in sediments near Haiphong Harbor, Vietnam. J Asian Earth Sci 56: 229–239. doi: 10.1016/j.jseaes.2012.05.015
|
| [56] | Sakan S, Sakan N, \DJor\d jević D (2015) Evaluation of the possibility of using normalization with cobalt in detection of anthropogenic heavy metals in sediments. Adv Chem Res 167–183. |
| [57] |
Matys Grygar T, Elznicová J, Bábek O, et al. (2014) Obtaining isochrones from pollution signals in a fluvial sediment record: A case study in a uranium-polluted floodplain of the Ploučnice River, Czech Republic. Appl Geochem 48: 1–15. doi: 10.1016/j.apgeochem.2014.06.021
|
| [58] | Buonicore AJ (1996) Cleanup Criteria for Contaminated Soil and Ground-water. ASTM International. |
| [59] | Chaerun SK, Whitman WB, Wirth SJ, Ellerbrock RH (2009) Chemical and Mineralogical Characterization of Agricultural Soils Inundated by the December 26, 2004 Tsunami after Intrinsic Bioremediation in Banda Aceh, Sumatra Island, Indonesia. In: Revitalizing the Environment: Proven Solutions and Innovative Approaches. American Society of Mining and Reclamation, Billings, MT, 210–226. |
| [60] | Kabata-Pendias A (2000) Trace Elements in Soils and Plants. CRC Press. |
| [61] |
Álvarez E, Fernández Marcos ML, Vaamonde C, et al. (2003) Heavy metals in the dump of an abandoned mine in Galicia (NW Spain) and in the spontaneously occurring vegetation. Sci Total Environ 313: 185–197. doi: 10.1016/S0048-9697(03)00261-4
|
| [62] | Ministry of the Environment F (2007) Government Decree on the Assessment of Soil Contamination and Remediation Needs 214/2007. Finnish and Swedish Ministry of the Environment, Finland. |
| [63] |
MacDonald DD, Ingersoll CG, Berger TA (2000) Development and Evaluation of Consensus-Based Sediment Quality Guidelines for Freshwater Ecosystems. Arch Environ Contam Toxicol 39: 20–31. doi: 10.1007/s002440010075
|
| [64] | Yates J (2017) The Effect of Organic Amendments on Soil Carbon Recovery in Reclaimed Mine Sites in Indonesia. Masters Thesis, Bangor University. |
| [65] |
Rädlein N, Heumann KG (1992) Trace Analysis of Heavy Metals in Aerosols Over the Atlantic Ocean from Antarctica to Europe. Int J Environ Anal Chem 48: 127–150. doi: 10.1080/03067319208027046
|
| [66] |
Reimann C, Caritat P de (2000) Intrinsic Flaws of Element Enrichment Factors (EFs) in Environmental Geochemistry. Environ Sci Technol 34: 5084–5091. doi: 10.1021/es001339o
|
| [67] |
Reimann C, de Caritat P (2005) Distinguishing between natural and anthropogenic sources for elements in the environment: regional geochemical surveys versus enrichment factors. Sci Total Environ 337: 91–101. doi: 10.1016/j.scitotenv.2004.06.011
|
| [68] |
Dung TTT, Cappuyns V, Swennen R, et al. (2013) From geochemical background determination to pollution assessment of heavy metals in sediments and soils. Rev Environ Sci Biotechnol 12: 335–353. doi: 10.1007/s11157-013-9315-1
|
| [69] |
Vaezi AR, Karbassi AR, Valavi Sh, et al. (2015) Ecological risk assessment of metals contamination in the sediment of the Bamdezh wetland, Iran. Int J Environ Sci Technol 12: 951–958. doi: 10.1007/s13762-014-0710-0
|
| [70] |
Chowdhury A, Maiti SK (2016) Identification of metal tolerant plant species in mangrove ecosystem by using community study and multivariate analysis: a case study from Indian Sunderban. Environ Earth Sci 75: 744–784. doi: 10.1007/s12665-016-5391-1
|
| [71] |
Peterson RK (2006) Comparing ecological risks of pesticides: the utility of a Risk Quotient ranking approach across refinements of exposure. Pest Manag Sci 62: 46–56. doi: 10.1002/ps.1126
|
| [72] |
Zhang Y, Liu Y, Niu Z, et al. (2017) Ecological risk assessment of toxic organic pollutant and heavy metals in water and sediment from a landscape lake in Tianjin City, China. Environ Sci Pollut Res 24: 12301–12311. doi: 10.1007/s11356-017-8906-8
|
| [73] |
Acevedo-Figueroa D, Jiménez BD, Rodríguez-Sierra CJ (2006) Trace metals in sediments of two estuarine lagoons from Puerto Rico. Environ Pollut 141: 336–342. doi: 10.1016/j.envpol.2005.08.037
|
| [74] |
Massas I, Kalivas D, Ehaliotis C, et al. (2013) Total and available heavy metal concentrations in soils of the Thriassio plan (Greece) and assessment of pollution indexes. Environ Monit Assess 185: 6751–6766. doi: 10.1007/s10661-013-3062-1
|
| [75] |
Tang Q, Li L, Zhang S, et al. (2018) Characterization of heavy metals in coal gangue-reclaimed soils from a coal mining area. J Geochem Explor 186: 1–11. doi: 10.1016/j.gexplo.2017.11.018
|
| [76] |
Wang L, Reddy KJ, Munn LC (1994) Geochemical modeling for predicting potential solid phases controlling the dissolved molybdenum in coal overburden, Powder River Basin, WY, U.S.A. Appl Geochem 9: 37–43. doi: 10.1016/0883-2927(94)90050-7
|
| [77] |
Humez N, Humez A-L, Juste C, et al. (1997) A new assessment of mobility of elements in sediments and wastes. Chem Speciat Bioavailab 9: 57–65. doi: 10.1080/09542299.1997.11083286
|
| [78] |
Kedziorek MAM, Dupuy A, Bourg ACM, et al. (1998) Leaching of Cd and Pb from a Polluted Soil during the Percolation of EDTA: Laboratory Column Experiments Modeled with a Non-Equilibrium Solubilization Step. Environ Sci Technol 32: 1609–1614. doi: 10.1021/es970708m
|
| [79] |
Kotková K, Nováková T, Tůmová Š, et al. (2019) Migration of risk elements within the floodplain of the Litavka River, the Czech Republic. Geomorphology 329: 46–57. doi: 10.1016/j.geomorph.2018.12.010
|
| [80] |
Noviyanto A, Purwanto P, Minardi S, et al. (2017) The assessment of soil quality of various age of land reclamation after coal mining: a chronosequence study. J Degraded Min Lands Manag Malang 5: 1009–1018. doi: 10.15243/jdmlm.2017.051.1009
|
| [81] |
Brantley SL, Lebedeva M (2011) Learning to Read the Chemistry of Regolith to Understand the Critical Zone. Annu Rev Earth Planet Sci 39: 387–416. doi: 10.1146/annurev-earth-040809-152321
|
| [82] |
Hudson‐Edwards KA, Macklin MG, Curtis CD, et al. (1998) Chemical remobilization of contaminant metals within floodplain sediments in an incising river system: implications for dating and chemostratigraphy. Earth Surf Proc Land 23: 671–684. doi: 10.1002/(SICI)1096-9837(199808)23:8<671::AID-ESP871>3.0.CO;2-R
|
| [83] | Fetter CW (2018) Applied Hydrogeology. Waveland Press. |
| [84] | Gasparatos D, Massas I, Godelitsas A (2019) Fe-Mn concretions and nodules formation in redoximorphic soils and their role on soil phosphorus dynamics: Current knowledge and gaps. Catena 182: 104–106. |
| [85] |
Dang Z, Liu C, Haigh MJ (2002) Mobility of heavy metals associated with the natural weathering of coal mine spoils. Environ Pollut 118: 419–426. doi: 10.1016/S0269-7491(01)00285-8
|
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| 33. | Natalie A. Harrison, Christopher L. Gardner, Danilo R. da Silva, Claudio F. Gonzalez, Graciela L. Lorca, Identification of Biomarkers for Systemic Distribution of Nanovesicles From Lactobacillus johnsonii N6.2, 2021, 12, 1664-3224, 10.3389/fimmu.2021.723433 | |
| 34. | Keita Nishiyama, Cheng-Chung Yong, Nobuko Moritoki, Haruki Kitazawa, Toshitaka Odamaki, Jin-Zhong Xiao, Takao Mukai, Danilo Ercolini, Sharing of Moonlighting Proteins Mediates the Symbiotic Relationship among Intestinal Commensals, 2023, 0099-2240, 10.1128/aem.02190-22 | |
| 35. | Przemysław Sałański, Magdalena Kowalczyk, Jacek K. Bardowski, Agnieszka K. Szczepankowska, Health-Promoting Nature of Lactococcus lactis IBB109 and Lactococcus lactis IBB417 Strains Exhibiting Proliferation Inhibition and Stimulation of Interleukin-18 Expression in Colorectal Cancer Cells, 2022, 13, 1664-302X, 10.3389/fmicb.2022.822912 | |
| 36. | Jia Wang, Yao Li, Longji Pan, Jun Li, Yanfei Yu, Beibei Liu, Muhammad Zubair, Yanna Wei, Bala Pillay, Ademola Olufolahan Olaniran, Thamsanqa E. Chiliza, Guoqing Shao, Zhixin Feng, Qiyan Xiong, Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) moonlights as an adhesin in Mycoplasma hyorhinis adhesion to epithelial cells as well as a plasminogen receptor mediating extracellular matrix degradation, 2021, 52, 1297-9716, 10.1186/s13567-021-00952-8 | |
| 37. | Tao Shi, Xi Guo, Yuqin Liu, Tingting Zhang, Xiangnan Wang, Zongjun Li, Yu Jiang, Rumen Metaproteomics Highlight the Unique Contributions of Microbe-Derived Extracellular and Intracellular Proteins for In Vitro Ruminal Fermentation, 2022, 8, 2311-5637, 394, 10.3390/fermentation8080394 | |
| 38. | Thomas B. Irving, Burcu Alptekin, Bailey Kleven, Jean‐Michel Ané, A critical review of 25 years of glomalin research: a better mechanical understanding and robust quantification techniques are required, 2021, 232, 0028-646X, 1572, 10.1111/nph.17713 | |
| 39. | Inés Reigada, Paola San-Martin-Galindo, Shella Gilbert-Girard, Jacopo Chiaro, Vincenzo Cerullo, Kirsi Savijoki, Tuula A. Nyman, Adyary Fallarero, Ilkka Miettinen, Surfaceome and Exoproteome Dynamics in Dual-Species Pseudomonas aeruginosa and Staphylococcus aureus Biofilms, 2021, 12, 1664-302X, 10.3389/fmicb.2021.672975 | |
| 40. | Jack A. Doolan, George T. Williams, Kira L. F. Hilton, Rajas Chaudhari, John S. Fossey, Benjamin T. Goult, Jennifer R. Hiscock, Advancements in antimicrobial nanoscale materials and self-assembling systems, 2022, 51, 0306-0012, 8696, 10.1039/D1CS00915J | |
| 41. | Yao Li, Jia Wang, Beibei Liu, Yanfei Yu, Ting Yuan, Yanna Wei, Yuan Gan, Jia Shao, Guoqing Shao, Zhixin Feng, Zhigang Tu, Qiyan Xiong, DnaK Functions as a Moonlighting Protein on the Surface of Mycoplasma hyorhinis Cells, 2022, 13, 1664-302X, 10.3389/fmicb.2022.842058 | |
| 42. | Yu Sun, Xuhang Wang, Qianwen Gong, Jin Li, Haosheng Huang, Feng Xue, Jianjun Dai, Fang Tang, Joanna B. Goldberg, Extraintestinal Pathogenic Escherichia coli Utilizes Surface-Located Elongation Factor G to Acquire Iron from Holo-Transferrin , 2022, 10, 2165-0497, 10.1128/spectrum.01662-21 | |
| 43. | Dorota Satala, Grzegorz Satala, Marcin Zawrotniak, Andrzej Kozik, Candida albicans and Candida glabrata triosephosphate isomerase – a moonlighting protein that can be exposed on the candidal cell surface and bind to human extracellular matrix proteins, 2021, 21, 1471-2180, 10.1186/s12866-021-02235-w | |
| 44. | Teresa Faddetta, Giovanni Renzone, Alberto Vassallo, Emilio Rimini, Giorgio Nasillo, Gianpiero Buscarino, Simonpietro Agnello, Mariano Licciardi, Luigi Botta, Andrea Scaloni, Antonio Palumbo Piccionello, Anna Maria Puglia, Giuseppe Gallo, Gladys Alexandre, Streptomyces coelicolor Vesicles: Many Molecules To Be Delivered, 2022, 88, 0099-2240, 10.1128/AEM.01881-21 | |
| 45. | Alain Filloux, Bacterial protein secretion systems: Game of types , 2022, 168, 1350-0872, 10.1099/mic.0.001193 | |
| 46. | Sébastien Massier, Brandon Robin, Marianne Mégroz, Amy Wright, Marina Harper, Brooke Hayes, Pascal Cosette, Isabelle Broutin, John D. Boyce, Emmanuelle Dé, Julie Hardouin, Phosphorylation of Extracellular Proteins in Acinetobacter baumannii in Sessile Mode of Growth, 2021, 12, 1664-302X, 10.3389/fmicb.2021.738780 | |
| 47. | Ana Luísa Matos, Pedro Curto, Isaura Simões, Moonlighting in Rickettsiales: Expanding Virulence Landscape, 2022, 7, 2414-6366, 32, 10.3390/tropicalmed7020032 | |
| 48. | Atsushi Kurata, Shimpei Takeuchi, Ryo Fujiwara, Kento Tamura, Tomoya Imai, Shino Yamasaki-Yashiki, Hiroki Onuma, Yasuhisa Fukuta, Norifumi Shirasaka, Koichi Uegaki, Activation of the toll-like receptor 2 signaling pathway by GAPDH from bacterial strain RD055328, 2023, 1347-6947, 10.1093/bbb/zbad059 | |
| 49. | Duoyi Hu, Irina Laczkovich, Michael J. Federle, Donald A. Morrison, Tina M. Henkin, Identification and Characterization of Negative Regulators of Rgg1518 Quorum Sensing in Streptococcus pneumoniae, 2023, 0021-9193, 10.1128/jb.00087-23 | |
| 50. | Jiah Yeom, Seongho Ma, Dong Joon Yim, Young-Hee Lim, Surface proteins of Propionibacterium freudenreichii MJ2 inhibit RANKL-induced osteoclast differentiation by lipocalin-2 upregulation and lipocalin-2-mediated NFATc1 inhibition, 2023, 13, 2045-2322, 10.1038/s41598-023-42944-y | |
| 51. | Ariana Casas-Román, María-José Lorite, Juan Sanjuán, María-Trinidad Gallegos, Two glyceraldehyde-3-phosphate dehydrogenases with distinctive roles in Pseudomonas syringae pv. tomato DC3000, 2024, 278, 09445013, 127530, 10.1016/j.micres.2023.127530 | |
| 52. | Dawei Chen, Congcong Guo, Chenyu Ren, Zihan Xia, Haiyan Xu, Hengxian Qu, Yunchao Wa, Chengran Guan, Chenchen Zhang, Jianya Qian, Ruixia Gu, Screening of Lactiplantibacillus plantarum 67 with Strong Adhesion to Caco-2 Cells and the Effects of Protective Agents on Its Adhesion Ability during Vacuum Freeze Drying, 2023, 12, 2304-8158, 3604, 10.3390/foods12193604 | |
| 53. | Rivesh Maharajh, Manormoney Pillay, Sibusiso Senzani, A computational method for the prediction and functional analysis of potential Mycobacterium tuberculosis adhesin-related proteins , 2023, 1478-9450, 1, 10.1080/14789450.2023.2275678 | |
| 54. | Nicole J. Curtis, Krupa J. Patel, Amina Rizwan, Constance J. Jeffery, Moonlighting Proteins: Diverse Functions Found in Fungi, 2023, 9, 2309-608X, 1107, 10.3390/jof9111107 | |
| 55. | Judeng Zeng, Chuan Xie, Ziheng Huang, Chi H. Cho, Hung Chan, Qing Li, Hassan Ashktorab, Duane T. Smoot, Sunny H. Wong, Jun Yu, Wei Gong, Cong Liang, Hongzhi Xu, Huarong Chen, Xiaodong Liu, Justin C. Y. Wu, Margaret Ip, Tony Gin, Lin Zhang, Matthew T. V. Chan, Wei Hu, William K. K. Wu, LOX-1 acts as an N6-methyladenosine-regulated receptor for Helicobacter pylori by binding to the bacterial catalase, 2024, 15, 2041-1723, 10.1038/s41467-024-44860-9 | |
| 56. | Amtul Jamil Sami, Sehrish Bilal, Sadaf Alam, Madeeha Khalid, Hammad Ahmad Mangat, A Method Based on a Modified Fluorescence In Situ Hybridization (FISH) Approach for the Sensing of Staphylococcus aureus from Nasal Samples, 2024, 0273-2289, 10.1007/s12010-024-04892-9 | |
| 57. | Ariana Casas-Román, María-José Lorite, Mariana Werner, Socorro Muñoz, María-Trinidad Gallegos, Juan Sanjuán, The gap gene of Rhizobium etli is required for both free life and symbiosis with common beans., 2024, 09445013, 127737, 10.1016/j.micres.2024.127737 | |
| 58. | Wenqian Liu, Zhen Wang, Shengjia Wang, Minghui Liu, Jian Zhang, Xuepeng Li, Hongye Wang, Jixing Feng, Identification of moonlighting adhesins of highly-adhesive Lactobacillus plantarum PO23 isolated from the intestine of Paralichthys olivaceus, 2024, 590, 00448486, 741044, 10.1016/j.aquaculture.2024.741044 | |
| 59. | Samuel A. Adeleye, Srujana S. Yadavalli, Jue D. Wang, Queuosine biosynthetic enzyme, QueE moonlights as a cell division regulator, 2024, 20, 1553-7404, e1011287, 10.1371/journal.pgen.1011287 | |
| 60. | Susan M. Noh, Jessica Ujczo, Debra C. Alperin, Identification of Anaplasma marginale adhesins for bovine erythrocytes using phage display, 2024, 5, 2673-7515, 10.3389/fitd.2024.1422860 | |
| 61. | Bruna Gonçalves, Diana Priscila Pires, Liliana Fernandes, Miguel Pacheco, Tiago Ferreira, Hugo Osório, Ana Raquel Soares, Mariana Henriques, Sónia Silva, Agostinho Carvalho, Biofilm matrix regulation by Candida glabrata Zap1 under acidic conditions: transcriptomic and proteomic analyses , 2024, 2165-0497, 10.1128/spectrum.01201-24 | |
| 62. | Ke Ma, Lei Deng, Yuanjie Wu, Yuan Gao, Jianhua Fan, Haizhen Wu, Transgenic Schizochytrium as a Promising Oral Vaccine Carrier: Potential Application in the Aquaculture Industry, 2024, 22, 1660-3397, 555, 10.3390/md22120555 | |
| 63. | Ana Carolina Franco Severo Martelli, Beatriz Brambila, Mariana Pegrucci Barcelos, Flávia da Silva Zandonadi, Solange Cristina Antão, André Vessoni Alexandrino, Carlos Henrique Tomich de Paula da Silva, Maria Teresa Marques Novo-Mansur, 2024, Chapter 10, 978-3-031-75983-3, 251, 10.1007/978-3-031-75984-0_10 | |
| 64. | Jizhen Cao, Han Li, Qing Han, Zhicheng Li, Jingyu Zhuang, Chuanfu Dong, Anxing Li, The accessory secretion system in Streptococcus agalactiae regulates protein secretion, stress resistance, adhesion, immune evasion, and virulence, 2025, 158, 10504648, 110172, 10.1016/j.fsi.2025.110172 | |
| 65. | Yinxiao Zhang, Yanchao Wen, Chi Zhang, Yuan Liu, Ran Wang, He Li, Xinqi Liu, Mechanisms of soybean proteins and peptides regulating the adhesion of Lacticaseibacillus rhamnosus GG and Lactiplantibacillus plantarum K25 to intestinal cells: A Comparative Study, 2025, 65, 22124292, 106156, 10.1016/j.fbio.2025.106156 | |
| 66. | Ran Wang, Yuan Liu, Yanchao Wen, Siyu Chen, Xiaohan Zhang, Chi Zhang, Xinqi Liu, Unraveling the secrets of probiotic adhesion: an overview of adhesion-associated cell surface components, adhesion mechanisms, and the effects of food composition, 2025, 09242244, 104945, 10.1016/j.tifs.2025.104945 | |
| 67. | Candelario Vazquez-Cruz, Edmundo Reyes-Malpica, J. Fernando Montes-García, Pamela Bautista-Betancourt, Elena Cobos-Justo, Miguel A. Avalos-Rangel, Erasmo Negrete-Abascal, Actinobacillus seminis DnaK interacts with bovine transferrin, lactoferrin, and hemoglobin as a putative iron acquisition mechanism, 2025, 0015-5632, 10.1007/s12223-025-01271-7 |
Figures(7) / Tables(5)
Jerry R. Miller, John P. Gannon, Kyle Corcoran. Concentrations, mobility, and potential ecological risks of selected metals within compost amended, reclaimed coal mine soils, tropical South Sumatra, Indonesia[J]. AIMS Environmental Science, 2019, 6(4): 298-325. doi: 10.3934/environsci.2019.4.298
| Protein | Species | UniProt ID | Extracellular function | References |
| 6-phosphofructokinase | Lactococcus lactis | P0DOB5 | yeast invertase | [54] |
| Streptococcus oralis | E6KMA1 | plasminogen | [78] | |
| Aaa autolysin | Staphylococcus aureus | Q2YVT4 | fibronectin | [37] |
| Aae autolysin | Staphylococcus epidermis | Q8CPQ1 | fibrinogen, fibronectin, vitronectin | [79] |
| Aspartase | Haemophilus influenzae | P44324 | plasminogen | [80] |
| Atla autolysin | Streptococcus mutans | U3SW74 | fibronectin | [39] |
| AtlC autolysin | Staphylococcus caprae | Q9AIS0 | fibronectin | [40] |
| Bile salt hydrolase | Bifidobacterium lactis | Q9KK62 | plasminogen | [81] |
| C5a peptidase | Streptococcus agalactiae | Q8E4T9 | fibronectin | [82] |
| DNA-directed RNA polymerase beta subunit | Streptococcus gordonii | A0EKJ1 | Muc7 | [18] |
| DnaK | Bifidobacterium | Q8G6W1 | plasminogen | [81] |
| Lactococcus lactis | P0A3J0 | yeast invertase | [54] | |
| Mycobacterium tuberculosis | A0A0H3L5C8 | plasminogen | [75] | |
| Neisseria meningitidis | A9M296 | plasminogen | [20] | |
| EF-Tu | Lactobacillus johnsonii | Q74JU6 | cells, mucins | [51] |
| Mycoplasma pneumoniae | P23568 | fibronectin, epithelial cells, plasminogen, heparin, fetuin, actin, fibrinogen, vitronectin, laminin | [36,64] | |
| Pseudonomas aeruginosa | P09591 | plasminogen | [43] | |
| Streptococcus gordonii | A8AWA0 | Muc7 | [18] | |
| Elongation factor G | Streptococcus gordonii | A8AUR6 | Muc7 | [18] |
| Endopeptidase O | Streptococcus pneumoniae | Q8DNW9 | plasminogen, fibronectin | [83] |
| Enolase | Aeromonas hydrophila | Q8GE63 | plasminogen | [22] |
| Bacillus anthracis | D8H2L1 | plasminogen, laminin | [8] | |
| Bifidobacterium lactis | B7GTK2 | plasminogen | [11] | |
| Borrelia burgdorferi | B7J1R2 | plasminogen | [16] | |
| Lactobacillus crispatus | Q5K117 | plasminogen, laminin | [14] | |
| Lactobacillus johnsonii | Q74K78 | plasminogen, laminin | [14] | |
| Lactobacillus plantarum | Q88YH3 | fibronectin | [23] | |
| Leishmania mexicana | Q3HL75 | plasminogen | [13] | |
| Mycoplasma fermentans | C4XEI3 | plasminogen | [24] | |
| Mycoplasma suis | F0QRW4 | red blood cells | [84] | |
| Mycoplasma synoviae | Q4A740 | plasminogen, fibronectin | [9] | |
| Neisseria meningitidis | E0N8L2 | plasminogen | [20] | |
| Staphylococcus aureus | Q6GB54 | plasminogen, laminin | [14,21] | |
| Streptococcus canis | I7WI49 | plasminogen | [17] | |
| Streptococcus gordonii | A8AY46 | Muc7 | [18] | |
| Streptococcus mutans | Q8DTS9 | plasminogen | [12] | |
| Streptococcus oralis | A0A1F1EC06 | plasminogen | [19] | |
| Streptococcus pneumoniae | Q97QS2 | plasminogen | [14] | |
| Streptococcus pyogenes | Q1JML5 | plasminogen | [14] | |
| Streptococcus suis | A4W2T1 | fibronectin, plasminogen | [15] | |
| Fructose 1,6-bisphosphate aldolase | Neisseria meningitidis | F0N9L0 | cells | [25] |
| GAPDH | Bacillus anthracis | Q81X74 | plasminogen | [85] |
| Lactobacillus acidophilus | Q5FL51 | mucin | [53] | |
| Lactobacillus plantarum | F9UM10 | mucin, Caco-2 cells | [50] | |
| Lactococcus lactis | P52987 | yeast invertase | [54] | |
| Mycoplasma genitalium | P47543 | mucin | [41] | |
| Staphylococcus aureus | Q6GIL8 | transferrin | [49] | |
| Streptococcus agalactiae | Q9ALW2 | plasminogen | [86] | |
| Streptococcus oralis | A0A0F2E7M6 | plasminogen | [78] | |
| Streptococcus pneumoniae | A0A0H2US80 | plasminogen | [87] | |
| Streptococcus pyogenes | P68777 | uPAR/CD87 receptor on human cells, plasminogen | [33,88] | |
| Streptococcus suis | Q3Y454 | plasminogen | [89] | |
| Glucose 6-phosphate isomerase | Lactobacillus crispatus | K1MKZ7 | laminin, collagen | [90] |
| Glutamine synthetase | Lactobacillus crispatus | D5GYN9 | fibronectin, laminin, collagen I, plasminogen | [90] |
| Mycobacterium tuberculosis | A0A0H3LHU4 | plasminogen, fibronectin | [91] | |
| Bifidobacterium lactis | C2GUH0 | plasminogen | [81] | |
| Hsp60 | Chlamydiae pneumoniae | P31681 | adhesin | [29] |
| Lactococcus lactis | P37282 | yeast invertase | [54] | |
| Legionella pneumophila | Q5X762 | adhesin | [30] | |
| Clostridium difficile | Q9KKF0 | adhesin | [27] | |
| Haemophilus ducreyi | P31294 | glycosphinngolipids | [34,35] | |
| Helicobacter pylori | Q8RNU2 | adhesin | [28] | |
| Lactobacillus johnsonii | F7SCR2 | adhesin | [52] | |
| Listeria | Q8KP52 | adhesin | [32] | |
| Salmonella typhimurium | P0A1D3 | mucus | [42] | |
| Hsp65/Cpn60.2/GroEL2 | Mycobacterium tuberculosis | A0A0H3LCC3 | CD43 on macrophage surface | [92] |
| Leucyl aminopeptidase | Mycoplasma hyopneumoniae | Q4A9M4 | heparin | [93] |
| Malate synthase | Mycobacterium tuberculosis | P9WK17 | fibronectin, laminin, epithelial cells | [38] |
| Glutamyl aminopeptidase | Mycoplasma hyopneumoniae | Q4AAK4 | plasminogen, heparin | [47] |
| Leucyl aminopeptidase | Mycoplasma hyopneumoniae | Q4A9M4 | plasminogen, heparin, DNA | [48] |
| Ornithine carbamoyltransferase | Staphylococcus epidermidis | P0C0N1 | fibronectin | [94] |
| Peroxiredoxin | Neisseria meningitidis | A0A125WDU3 | plasminogen | [20] |
| Streptococcus agalactiae | E7S2A7 | heme | [95] | |
| Phosphoglycerate kinase | Streptococcus oralis | A0A0G7HBY7 | plasminogen | [77] |
| Streptococcus agalactiae | Q8DXT0 | plasminogen, actin | [83,96] | |
| Streptococcus pneumoniae | Q8DQX8 | plasminogen | [97] | |
| Phosphoglycerate mutase | Bifidobacterium lactis | P59159 | plasminogen | [81] |
| Streptococcus oralis | E6IYJ0 | plasminogen | [78] | |
| Pyruvate dehydrogenase | Mycoplasma pneumoniae | P75391 | fibrinogen | [36] |
| Pyruvate kinase | Lactococcus lactis | Q07637 | yeast invertase | [54] |
| Superoxide dismutase | Mycobacterium avium | P53647 | adhesin | [98] |
| Triose phosphate isomerase | Streptococcus oralis | E6J203 | plasminogen | [78] |
DownLoad: CSV| Protein | Species | UniProt ID | Extracellular function | References |
| 6-phosphofructokinase | Lactococcus lactis | P0DOB5 | yeast invertase | [54] |
| Streptococcus oralis | E6KMA1 | plasminogen | [78] | |
| Aaa autolysin | Staphylococcus aureus | Q2YVT4 | fibronectin | [37] |
| Aae autolysin | Staphylococcus epidermis | Q8CPQ1 | fibrinogen, fibronectin, vitronectin | [79] |
| Aspartase | Haemophilus influenzae | P44324 | plasminogen | [80] |
| Atla autolysin | Streptococcus mutans | U3SW74 | fibronectin | [39] |
| AtlC autolysin | Staphylococcus caprae | Q9AIS0 | fibronectin | [40] |
| Bile salt hydrolase | Bifidobacterium lactis | Q9KK62 | plasminogen | [81] |
| C5a peptidase | Streptococcus agalactiae | Q8E4T9 | fibronectin | [82] |
| DNA-directed RNA polymerase beta subunit | Streptococcus gordonii | A0EKJ1 | Muc7 | [18] |
| DnaK | Bifidobacterium | Q8G6W1 | plasminogen | [81] |
| Lactococcus lactis | P0A3J0 | yeast invertase | [54] | |
| Mycobacterium tuberculosis | A0A0H3L5C8 | plasminogen | [75] | |
| Neisseria meningitidis | A9M296 | plasminogen | [20] | |
| EF-Tu | Lactobacillus johnsonii | Q74JU6 | cells, mucins | [51] |
| Mycoplasma pneumoniae | P23568 | fibronectin, epithelial cells, plasminogen, heparin, fetuin, actin, fibrinogen, vitronectin, laminin | [36,64] | |
| Pseudonomas aeruginosa | P09591 | plasminogen | [43] | |
| Streptococcus gordonii | A8AWA0 | Muc7 | [18] | |
| Elongation factor G | Streptococcus gordonii | A8AUR6 | Muc7 | [18] |
| Endopeptidase O | Streptococcus pneumoniae | Q8DNW9 | plasminogen, fibronectin | [83] |
| Enolase | Aeromonas hydrophila | Q8GE63 | plasminogen | [22] |
| Bacillus anthracis | D8H2L1 | plasminogen, laminin | [8] | |
| Bifidobacterium lactis | B7GTK2 | plasminogen | [11] | |
| Borrelia burgdorferi | B7J1R2 | plasminogen | [16] | |
| Lactobacillus crispatus | Q5K117 | plasminogen, laminin | [14] | |
| Lactobacillus johnsonii | Q74K78 | plasminogen, laminin | [14] | |
| Lactobacillus plantarum | Q88YH3 | fibronectin | [23] | |
| Leishmania mexicana | Q3HL75 | plasminogen | [13] | |
| Mycoplasma fermentans | C4XEI3 | plasminogen | [24] | |
| Mycoplasma suis | F0QRW4 | red blood cells | [84] | |
| Mycoplasma synoviae | Q4A740 | plasminogen, fibronectin | [9] | |
| Neisseria meningitidis | E0N8L2 | plasminogen | [20] | |
| Staphylococcus aureus | Q6GB54 | plasminogen, laminin | [14,21] | |
| Streptococcus canis | I7WI49 | plasminogen | [17] | |
| Streptococcus gordonii | A8AY46 | Muc7 | [18] | |
| Streptococcus mutans | Q8DTS9 | plasminogen | [12] | |
| Streptococcus oralis | A0A1F1EC06 | plasminogen | [19] | |
| Streptococcus pneumoniae | Q97QS2 | plasminogen | [14] | |
| Streptococcus pyogenes | Q1JML5 | plasminogen | [14] | |
| Streptococcus suis | A4W2T1 | fibronectin, plasminogen | [15] | |
| Fructose 1,6-bisphosphate aldolase | Neisseria meningitidis | F0N9L0 | cells | [25] |
| GAPDH | Bacillus anthracis | Q81X74 | plasminogen | [85] |
| Lactobacillus acidophilus | Q5FL51 | mucin | [53] | |
| Lactobacillus plantarum | F9UM10 | mucin, Caco-2 cells | [50] | |
| Lactococcus lactis | P52987 | yeast invertase | [54] | |
| Mycoplasma genitalium | P47543 | mucin | [41] | |
| Staphylococcus aureus | Q6GIL8 | transferrin | [49] | |
| Streptococcus agalactiae | Q9ALW2 | plasminogen | [86] | |
| Streptococcus oralis | A0A0F2E7M6 | plasminogen | [78] | |
| Streptococcus pneumoniae | A0A0H2US80 | plasminogen | [87] | |
| Streptococcus pyogenes | P68777 | uPAR/CD87 receptor on human cells, plasminogen | [33,88] | |
| Streptococcus suis | Q3Y454 | plasminogen | [89] | |
| Glucose 6-phosphate isomerase | Lactobacillus crispatus | K1MKZ7 | laminin, collagen | [90] |
| Glutamine synthetase | Lactobacillus crispatus | D5GYN9 | fibronectin, laminin, collagen I, plasminogen | [90] |
| Mycobacterium tuberculosis | A0A0H3LHU4 | plasminogen, fibronectin | [91] | |
| Bifidobacterium lactis | C2GUH0 | plasminogen | [81] | |
| Hsp60 | Chlamydiae pneumoniae | P31681 | adhesin | [29] |
| Lactococcus lactis | P37282 | yeast invertase | [54] | |
| Legionella pneumophila | Q5X762 | adhesin | [30] | |
| Clostridium difficile | Q9KKF0 | adhesin | [27] | |
| Haemophilus ducreyi | P31294 | glycosphinngolipids | [34,35] | |
| Helicobacter pylori | Q8RNU2 | adhesin | [28] | |
| Lactobacillus johnsonii | F7SCR2 | adhesin | [52] | |
| Listeria | Q8KP52 | adhesin | [32] | |
| Salmonella typhimurium | P0A1D3 | mucus | [42] | |
| Hsp65/Cpn60.2/GroEL2 | Mycobacterium tuberculosis | A0A0H3LCC3 | CD43 on macrophage surface | [92] |
| Leucyl aminopeptidase | Mycoplasma hyopneumoniae | Q4A9M4 | heparin | [93] |
| Malate synthase | Mycobacterium tuberculosis | P9WK17 | fibronectin, laminin, epithelial cells | [38] |
| Glutamyl aminopeptidase | Mycoplasma hyopneumoniae | Q4AAK4 | plasminogen, heparin | [47] |
| Leucyl aminopeptidase | Mycoplasma hyopneumoniae | Q4A9M4 | plasminogen, heparin, DNA | [48] |
| Ornithine carbamoyltransferase | Staphylococcus epidermidis | P0C0N1 | fibronectin | [94] |
| Peroxiredoxin | Neisseria meningitidis | A0A125WDU3 | plasminogen | [20] |
| Streptococcus agalactiae | E7S2A7 | heme | [95] | |
| Phosphoglycerate kinase | Streptococcus oralis | A0A0G7HBY7 | plasminogen | [77] |
| Streptococcus agalactiae | Q8DXT0 | plasminogen, actin | [83,96] | |
| Streptococcus pneumoniae | Q8DQX8 | plasminogen | [97] | |
| Phosphoglycerate mutase | Bifidobacterium lactis | P59159 | plasminogen | [81] |
| Streptococcus oralis | E6IYJ0 | plasminogen | [78] | |
| Pyruvate dehydrogenase | Mycoplasma pneumoniae | P75391 | fibrinogen | [36] |
| Pyruvate kinase | Lactococcus lactis | Q07637 | yeast invertase | [54] |
| Superoxide dismutase | Mycobacterium avium | P53647 | adhesin | [98] |
| Triose phosphate isomerase | Streptococcus oralis | E6J203 | plasminogen | [78] |
