Research article

Concentrations, mobility, and potential ecological risks of selected metals within compost amended, reclaimed coal mine soils, tropical South Sumatra, Indonesia

  • Coal production in tropical areas of southeast Asia, the majority by opencast mining, has grown exponentially since the late 20th century, raising concerns about its impacts on terrestrial and aquatic ecosystems. In this study, potential impacts of six metals (Al, Fe, Mn, Ni, Pb, Zn) in reclaimed mine soils amended with compost were examined at the PT Bukit Asam-Tanjung Enim mine in South Sumatra, Indonesia. The analysis was carried out by measuring and comparing metal concentrations in the soil matrix and soil waters at three reclaimed sites of differing age and compost treatments. Calculated soil enrichment factors and risk quotients (for water and soil) based on multiple background and toxicity criteria suggest the risk posed by metals within the reclaimed soils and soil water was negligible. Differences between treated and untreated sites suggest the influence of organic matter (OM) on dissolved metal concentrations varied between metals. Insignificant statistical differences (P < 0.05) in dissolved Mn or Zn concentrations between control and compost treated sites suggest that dissolved organic carbon (DOC) did not influence Mn or Zn soil water concentrations. In contrast, control plots had the lowest dissolved soil water concentrations of Al, Fe, and Pb; maximum concentrations were measured at a 1-year old compost-amended site whose soils had the highest C contents. These data suggest that the dissolution of OM, and the formation of DOC, may have increased the solubility of Al, Fe, and Pb within the reclaimed soils. However, no significant differences in metal concentrations were observed between surface- and subsurface soil layers, suggesting that migration was limited at all sites, including those treated with compost. Metal mobility and risks were likely reduced by multiple factors, including (1) relatively low metal concentrations and a lack of acid-producing sulfide minerals in the reclaimed topsoil, and (2) the fine-grained nature of the reclaimed soils, which limited the rate of soil water flow and increased the sorption potential of the soil matrix.

    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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  • Coal production in tropical areas of southeast Asia, the majority by opencast mining, has grown exponentially since the late 20th century, raising concerns about its impacts on terrestrial and aquatic ecosystems. In this study, potential impacts of six metals (Al, Fe, Mn, Ni, Pb, Zn) in reclaimed mine soils amended with compost were examined at the PT Bukit Asam-Tanjung Enim mine in South Sumatra, Indonesia. The analysis was carried out by measuring and comparing metal concentrations in the soil matrix and soil waters at three reclaimed sites of differing age and compost treatments. Calculated soil enrichment factors and risk quotients (for water and soil) based on multiple background and toxicity criteria suggest the risk posed by metals within the reclaimed soils and soil water was negligible. Differences between treated and untreated sites suggest the influence of organic matter (OM) on dissolved metal concentrations varied between metals. Insignificant statistical differences (P < 0.05) in dissolved Mn or Zn concentrations between control and compost treated sites suggest that dissolved organic carbon (DOC) did not influence Mn or Zn soil water concentrations. In contrast, control plots had the lowest dissolved soil water concentrations of Al, Fe, and Pb; maximum concentrations were measured at a 1-year old compost-amended site whose soils had the highest C contents. These data suggest that the dissolution of OM, and the formation of DOC, may have increased the solubility of Al, Fe, and Pb within the reclaimed soils. However, no significant differences in metal concentrations were observed between surface- and subsurface soil layers, suggesting that migration was limited at all sites, including those treated with compost. Metal mobility and risks were likely reduced by multiple factors, including (1) relatively low metal concentrations and a lack of acid-producing sulfide minerals in the reclaimed topsoil, and (2) the fine-grained nature of the reclaimed soils, which limited the rate of soil water flow and increased the sorption potential of the soil matrix.


    1. Introduction to intracellular proteins that moonlight as bacterial adhesins

    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].


    2. Importance in health and disease

    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].


    3. Proteomic and other technical approaches for identifying intracellular/surface proteins

    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.


    4. Molecular mechanisms for intracellular proteins to function as cell surface adhesins

    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].


    5. Potential for targeting ISMPs in the development of novel antibacterials and treatments for IBD

    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.

    Table 1. Intracellular proteins that function as cell surface adhesins in bacteria.
    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]
     | Show Table
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    6. Conclusions

    The 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.


    Conflict of interest

    The author declares no conflict of interest in this paper.




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