Research article

Substrate preferences, phylogenetic and biochemical properties of proteolytic bacteria present in the digestive tract of Nile tilapia (Oreochromis niloticus)

  • Vertebrate intestine appears to be an excellent source of proteolytic bacteria for industrial and probiotic use. We therefore aimed at obtaining the gut-associated proteolytic species of Nile tilapia (Oreochromis niloticus). We have isolated twenty six bacterial strains from its intestinal tract, seven of which showed exoprotease activity with the formation of clear halos on skim milk. Their depolymerization ability was further assessed on three distinct proteins including casein, gelatin, and albumin. All the isolates could successfully hydrolyze the three substrates indicating relatively broad specificity of their secreted proteases. Molecular taxonomy and phylogeny of the proteolytic isolates were determined based on their 16S rRNA gene barcoding, which suggested that the seven strains belong to three phyla viz. Firmicutes, Proteobacteria, and Actinobacteria, distributed across the genera Priestia, Citrobacter, Pseudomonas, Stenotrophomonas, Burkholderia, Providencia, and Micrococcus. The isolates were further characterized by a comprehensive study of their morphological, cultural, cellular and biochemical properties which were consistent with the phylogenetic annotations. To reveal their proteolytic capacity alongside substrate preferences, enzyme-production was determined by the diffusion assay. The Pseudomonas, Stenotrophomonas and Micrococcus isolates appeared to be most promising with maximum protease production on casein, gelatin, and albumin media respectively. Our findings present valuable insights into the phylogenetic and biochemical properties of gut-associated proteolytic strains of Nile tilapia.

    Citation: Tanim Jabid Hossain, Mukta Das, Ferdausi Ali, Sumaiya Islam Chowdhury, Subrina Akter Zedny. Substrate preferences, phylogenetic and biochemical properties of proteolytic bacteria present in the digestive tract of Nile tilapia (Oreochromis niloticus)[J]. AIMS Microbiology, 2021, 7(4): 528-545. doi: 10.3934/microbiol.2021032

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  • Vertebrate intestine appears to be an excellent source of proteolytic bacteria for industrial and probiotic use. We therefore aimed at obtaining the gut-associated proteolytic species of Nile tilapia (Oreochromis niloticus). We have isolated twenty six bacterial strains from its intestinal tract, seven of which showed exoprotease activity with the formation of clear halos on skim milk. Their depolymerization ability was further assessed on three distinct proteins including casein, gelatin, and albumin. All the isolates could successfully hydrolyze the three substrates indicating relatively broad specificity of their secreted proteases. Molecular taxonomy and phylogeny of the proteolytic isolates were determined based on their 16S rRNA gene barcoding, which suggested that the seven strains belong to three phyla viz. Firmicutes, Proteobacteria, and Actinobacteria, distributed across the genera Priestia, Citrobacter, Pseudomonas, Stenotrophomonas, Burkholderia, Providencia, and Micrococcus. The isolates were further characterized by a comprehensive study of their morphological, cultural, cellular and biochemical properties which were consistent with the phylogenetic annotations. To reveal their proteolytic capacity alongside substrate preferences, enzyme-production was determined by the diffusion assay. The Pseudomonas, Stenotrophomonas and Micrococcus isolates appeared to be most promising with maximum protease production on casein, gelatin, and albumin media respectively. Our findings present valuable insights into the phylogenetic and biochemical properties of gut-associated proteolytic strains of Nile tilapia.



    Nitric oxide (NO) is a gaseous chemical messenger that participates in varied physiological functions [1],[2]. In line with the widespread expression of this pathway, NO participates in various brain functions. NO regulates the activity of neurotransmitter systems of the brain and the content of neuromediators in the extracellular space [3],[4]. The role of NO as a biological messenger is determined primarily by its physicochemical properties. It is a highly labile, short-living, reactive free radical [5],[6]. The conclusion that NO is a regulatory molecule possessing the properties of a biological messenger was a consequence of the development of numerous scientific fields, including the physiology and pharmacology of the cardiovascular system, toxicology, neurobiology, etc. In recent decades, the role of NO was shown in modeling of central nervous system diseases such as neurodegenerative disorders, stroke, epilepsy, neurotoxic damage [7][12].

    The property of NO to cause a biological effect depends to a large extent on the small size of its molecule, its high reactivity, and its ability to diffuse in tissues, including the nervous system. This was the reason to call NO a retrograde messenger [13]. Recently, the importance of NO as a universal modulator in the brain has been postulated [2]. This compound is formed from L-arginine as a result of a two-step reaction of the enzymatic oxidation of its guanidine group to form an intermediate, NG-hydroxy-L-arginine. Several isoforms of NO-synthase (NOS) have been described: constitutive, permanently present in tissue and inducible. Thereby, activity of NOS is important for the manifestation of the physiological and neurochemical action of NO [14],[15].

    Amphetamine-like psychostimulants, such as amphetamine (AMPH), 3,4-methylenedioxymethamphetamine (MDMA or Ecstasy), and methamphetamine (METH) are psychomotor stimulants that may cause addiction [16]. The mechanism of action of AMPH -like psychostimulants is associated with their ability to influence the monoaminergic systems of the brain. AMPH and its derivatives have a pronounced neurotoxic potential, which is manifested, in particular, in reducing the neuronal content of dopamine (DA), reducing the number of binding sites of the synaptic dopamine transporter [17], degeneration of dopaminergic terminals of the nigrostriatal system [18][21]. Recent reports claim that other brain neurotransmitters, such as glutamate and acetylcholine (ACH) are also involved in the mechanism of neurotoxicity evoked by psychostimulant [2],[22][24].

    The precise mechanisms of AMPH-induced neurotoxicity remain unclear. Characteristic manifestations of the neurotoxic effect of AMPH and its derivatives, along with the depletion of intracellular DA and degeneration of neurons, are considered to be due to an generation of reactive oxygen species (ROS) and reactive nitrogen species (RNS [25][28]. Significant intensification of lipid peroxidation (LPO) processes in the brain was detected after a single injection of METH [29]. Increased generation of hydroxyl radicals as well as elevation of LPO products in rat striatum after AMPH administration has been observed [30]. Similar changes in hydroxyl radicals and LPO have been previously described during convulsions of various genesis as well as during global ischemia in rats [31][33]. It has been suggested that NOS inhibitor methyl N-nitro-L-arginine ester (L-NAME) [34], or neuronal NOS inhibitor (nNOS) 7-nitroindazole (7-NI) [35] prevent neurotoxic effects of AMPH-like psychostimulants in rats. L-NAME abolishes sensitization to AMPH after short-term and long-term withdrawal [36]. It has also been shown that treatment of newborns with a non-specific NOS inhibitor causes a long-term alternation in the content of NO in the brain with possible consequences for the transmission of DA [37]. Using immunocytochemistry and double in situ hybridization it has been demonstrated that serotonin neurones, which express NOS, are most vulnerable to toxicity induced by substitutes of AMPH such as 3,4-methylenedioxymethamphetamine and p-chloroamphetamine [38]. Furthermore, it has been shown that effects of AMPH on basal nNOS mRNA expression in neurons containing nNOS in the striatum depends on dose of the drug [39]. Similarly, the effect of AMPH on the increase in inducible NOS mRNA (iNOS) in highly agammaessive proliferating immortalized microglia cells is also concenraion-dependent. [40]. Furthermore, it has been shown that repeated administration of MDMA elevates nNOS in the nigrostriatal system.

    Aim of this review is to describe the involvement of NO and the contribution of LPO and ACH release in neurotoxic effects elicited by psychostimulant drugs. Furthermore, the effects of equimolar concentrations AMPH and the psychostimulant sydnocrab in on the levels of NO and LPO products in rat brain structures will be delineated.

    NO levels were determined by electron paramagnetic resonance (EPR). This method allows to determine NO in vivo as a paramagnetic complex in organs and tissues, e.g. liver, heart, tumor etc. [41][43]. The method was slightly modified for detection of NO in brain structures of rats [44]. For our purposes, selective scavenger of NO diethyldithiocarbamate (Sigma, 500 mg/kg, i.p.) and a mixture of FeSO4 (37.5 mg/kg, s.c.) and sodium citrate (165 mg/kg, s.c.) were injected simultaneously and animals were decapitated after 30 minutes. The EPR spectra were recorded at 77 K using a Brucker ESR 300E spectrometer at a frequency of 9.33 kHz, hf-modulation frequency 0.5 mT, microwave power 20 mW and time constant 0.05 s. The concentration of trapped NO was calculated from the intensity of the third ultrafine splitting line of the resonance at g = 2.035.

    We used the following two approaches to study the participation of NO in the development of neurotoxicity evoked by psychomotor stimulants.

    Experiments were carried out on a male Sprague-Dawley rats (280–300 g) from the vivarium of University of Innsbruck. Protocols were approved by the Bundesministerium für Wissenschaft, Forschung und Kunst, Austria, Kommission für Tierversuchsangelegenheiten. Rats were injected with AMPH (Merck, Darmstadt, Germany) four times. The EPR signals of paramagnetic mononitrosyl MNIC–DETC complex registered in the brain cortex of rats are shown in Figure 1. The EPR signal, which represents NO, was enhanced following AMPH administration [45].

    Repeated, systemic application of AMPH elevated striatal and cortical NO content (Figure 2A). Administration of the non-competitive NOS inhibitor N-nitro-L-arginine (L-NNA: Sigma, Deisenhofen, Germany) reduced but not abolished the elevation in NO levels evoked by AMPH. Similarly, the selective nNOS inhibitor 7-Nitroindazole (7-NI) (Sigma, Germany) significantly attenuated the AMPH induced NO generation [46]. The findings demonstrate that endogenous NO is implicated in neurotoxicity elicited by AMPH-like psychostimulants.

    Figure 1.  Typical EPR spectra of the cerebral cortex after administration of DETC and Fe citrate 30 min prior to decapitation. The signals at g, g|| and g are due to NO-Fe-DETC and reduced iron-sulfur proteins in the mitochondrion respiratory chain. The arrows A, B, C and D indicate the position of components of ultrafine structure of EPR signals from Cu2+-DETC complexes at g. Arrow direction of B extension of magnetic field [reproduced from Bashkatova et al., 1999].

    The interaction of NO with the neurotransmitter glutamate prompted us to study the possible role of this messenger in the pathophysiological mechanisms of AMPH-induced neurotoxicity. The inhibitor of NMDA glutamate receptors dizocilpine (MK-801, Research Biochemical International, Natick, MA, U.S.A.) was administered 30 min prior first AMPH injection. Dizocilpine abolished the rise of NO content induced by four injections of the psychostimulant (Figure 2A) [47]. This finding indicates that NMDA receptors mediate AMPH neurotoxicity and that, as already mentioned, NO is involved in this process.

    NO might interact with other radicals, such as ROS. It is known that high doses of AMPH - like psychostimulants lead to an increase in the levels of hydroxyl radicals and LPO products in rat brain [48],[49]. Interaction of NO with ROS causes the generation of highly toxic products, in particular, peroxynitrite, which leads to damage and death of neurons [50][52]. However, the possible relationship of these processes is poorly understood. Intensity of LPO processes in brain areas was determined by measuring thiobarbituric acid reactive substances (TBARS). Briefly, tissue homogenate was mixed with sodium dodecyl sulfate, acetate buffer and thiobarbituric acid. After heating, the pigment was extracted with n-butanol-pyridine mixture and the absorbency was determined at 532 nm [53]. After the last injection of AMPH a more than two-fold increase in TBARSlevel in the striatum and in the cortex was found [46] (Figure 2B). The NOS inhibitors (L-NNA or 7-NI) administered prior to AMPH failed the increase either striatal, or cortical content of TBARS (Figure 2B). Pretreatment with dizocilpine abolished AMPH-induced elevation of LPO levels in both brain areas (Figure 2B).

    These findings are in accordance with our results carried out on the seizure models of rats [54],[55] and indicate that both the NO and NO-independent LPO are involved in the neurotoxicity caused by AMPH.

    Figure 2.  Effect of NOS inhibitors (L-NNA, 100 mg/kg, i.p., n = 7 and 7-NI, 50 mg/kg, i.p., n = 6) and NMDA antagonist dizocilpine (1 mg/kg, i.p., n = 6) injected 30 min prior the 1st AMPH injection (5 mg/kg, i.p., injected 4 times every 2 h, n = 6) on NO generation [A] and TBARS content [B] in striatum and cortex of rats. Data are the mean ± SEM. n = amount of rats/group. *P < 0.05, **P < 0.01 compared with the control (vehicle) group; #P < 0.05, ##P < 0.01 compared with AMPH treated rats [to be published].

    In our experiments the push-pull superfusion technique was used that makes it possible to determine quantitatively ACH released from their neurons in the synaptic cleft in distinct brain areas [47],[56]. For the determination of ACH release in the Nac the animals were anaesthetized with urethane, the head was fixed in a stereotaxic frame, and a push-pull cannula (outer tubing: outer diameter 0.83 mm, inner diameter 0.51 mm; inner tubing: outer diameter 0.31 mm, inner diameter 0.16 mm) was stereotaxically inserted through a hole in the skull into the Nac. The Nac was superfused with artificial cerebrospinal fluid which additionally contained neostigmine. The superfusate was continuously collected in time periods of 10 min. The superfusion rate was 20 µl/min. At the end of the experiment the rat was killed with an overdose of sodium phenobarbital and the brain was removed and immersed in formaldehyde solution. ACH was determined in the superfusate by high pressure liquid chromatography (HPLC) with electrochemical detection [56].

    The mean basal output of ACH in the nucleus accumbens (NAc) was found to be 25.1 ± 9.1 fmol min−1. Four injections of the vehicle did not influence the release of ACH (Figure 3), while four repeated injections of AMPH led to a dramatic increase in the ACH release rates. The enhanced ACH release reached its maximum 40–120 min after administration of AMPH and persisted to the end of the experiment. NOS inhibitors (Figure 3) as well as the NMDA antagonist (Figure 4) almost completely prevented the increase of ACH release evoked by AMPH.

    Very probably, the increase in ACH release following AMPH administration is due to the activation of nNOS. Moreover, the findings point to the crucial role of nNOS in the neurotoxic effects of AMPH. It is still controversial whether NO is functioning as protective agent against neurotoxic effects of AMPH [3],[57]. Our results underpin the idea that NO formation prevents neurotoxicity elucidated be AMPH [58].

    It has been suggested that glutamatergic neurotransmission is involved in neurotoxicity elicited by AMPH [59][61]. As already mentioned (see 2.1.), the antagonist of NMDA receptor dizocilpine was very effective in reducing the ACH release caused by AMPH. Furthermore, dizocilpine prevented the increase of NO and LPO levels evoked by AMPH. Our results are in accordance with the observation that both NO and NMDA glutamate receptors are implicated in depressive conditions after amphetamine withdrawal [62]. Taken together, the data suggest that activation of NMDA receptors is necessary to induce AMPH neurotoxicity and to modify processes of neurotransmission within NAc.

    In clinical practice, the administration of psychostimulants is limited due to a number of side effects. including their neurotoxic action. However, administration of psychostimulants is necessary for the treatment of a number of diseases of the central nervous system, especially in the case of attention deficit hyperactivity syndrome [63][65]. In this regard, the search for new drugs with psychostimulating action, but with less neurotoxicity than amphetamine, is one of the actual problems of modern pharmacology. Sydnocarb (*-phenylisopropyl) -N-phenylcarbamoyl sidnonimine), like other indirect dopaminomimetics, has a wide range of psychoactive properties [66][68]. Comparison of sydnocarb with METH has shown that the dysfunction of dopaminergic neurotransmission elicited by sydnocarb occurred more slowly and gradually than that of METH [69].

    EPR technique was used to compare the effects of two psychostimulant drugs, AMPH and sydnocarb, at the equimolar doses (5 and 23.8 mg/kg, respectively) on the NO level in striatum and cortex of male Sprague Dawley rats (180–210 g) [70]. All experiments were performed in accordance with the French decree No. 87848/19 October 1987 and associated guidelines and the European Community Council directive 86/609/EEC/November 1986 (that corresponds to the recent Directive 2010/63/EU). AMPH greatly increased NO levels in the striatum and in the cortex of rats two hours after injection. Sydnocarb also increased NO content, however to a lesser extent than AMPH. Moreover, AMPH evoked more pronounced elevation of LPO products than sydnocarb in both brain areas. Hence, sydnocarb seems to be less neurotoxic than AMPH [70].

    Figure 3.  Effects of AMPH, of L-NNA and 7-NI on the release of ACH in the Nac. Arrows indicate injections of AMPH (5 mg/kg, i.p.), L-NNA (100 mg/kg, i.p.) and 7-NI (50 mg/kg, i.p.) were administered 30 min prior to the first injection of AMPH. The basal release rate in two samples preceding the first injection of AMPH was taken as 1. *P < 0.05 versus controls. Mean values ± s.e.m., n = 4–6 rats/group. Compounds were administered i.p. so as to make possible comparisons with other findings and to avoid interferences with other factors such as differing absortion rates [reproduced from Bashkatova et al., 1999].
    Figure 4.  Effects of AMPH and dizocilpine (MK-801) on the release of ACH in the Nac. Arrows indicate injections of AMPH (5 mg/kg, i.p.). Dizocilpine (1 mg/kg, i.p.) was administered 30 min prior to the first injection of AMPH. The basal release rate in two samples preceding the first injection of AMPH was taken as 1. *P < 0.05 versus controls. Mean values ± s.e.m., n = 4–6 rats/group (reproduced from Kraus et al., 2002).

    These findings are consistent with recent studies that AMPH has a significantly higher impact on the parameters of the stereotypical behavior of rats [71]. The maximum level of stereotypy (6 scores) was achieved within 2 hours after the first injection of the drug. Sydnocarb also caused motor stereotypy, but its intensity was significantly lower than that of AMPH (4 scores). Moreover, sydnocarb led to a slow and gradual increase of the parameters of dopaminergic dysfunction in comparison with AMPH [72]. Moreover, treatment with sydnocarb was accompanied by a less pronounced increase in formation of OH in comparison with that after AMPH administration [73]. It has been established that increased formation of free radicals induces LPO, which is considered to be one of indexes of neurotoxicity [74],[75]. Our findings demonstrate that AMPH as well as sydnocarb enhance NO generation and TBARS formation in rat brain. Finally, our results suggest that in striatum and cerebral cortex, AMPH, and to a lesser degree sydnocarb, may elicit neurotoxicity.

    Taken together, these findings confirm that NO and ROS play important role in processes of neurotoxicity evoked by AMPH and sydnocarb. Furthermore, they point to the key role of neuronal NOS in AMPH- induced neurotoxicity and demonstrate the crucial role of NO in neurotoxicity induced by psychostimulant drugs.


    Acknowledgments



    We are grateful to Prof. Dr. Md. Monirul Islam, Dept. of Biochemistry and Molecular Biology, University of Chittagong (BMB, CU) for his kind support with laboratory equipment. We thank members of the Biochemistry and Pathogenesis of Microbes–BPM Research Group, BMB, CU for their various help in this project.

    Author contributions



    TJH conceived and designed the study; MD, FA, TJH and SIC performed experiments; SIC contributed to sequence study and TJH performed the phylogenetic analysis; TJH and FA interpreted the data; TJH wrote and prepared the manuscript; SAZ assisted in writing introduction; SAZ and FA helped in information collection; all authors approved the final manuscript.

    Funding



    This research was supported by University of Chittagong via its Planning and Development Department to TJH.

    Conflict of interest



    The authors have no conflicts of interest to declare.

    Ethical approval



    This article does not contain any experiments performed on human participants or animals by any of the authors.

    [1] Jakubke HD, Kuhl P, Könnecke A (1985) Basic Principles of protease-catalyzed peptide bond formation. Angewandte Chemie International Edition in English 24: 85-93. doi: 10.1002/anie.198500851
    [2] Gupta R, Beg Q, Lorenz P (2002) Bacterial alkaline proteases: molecular approaches and industrial applications. Appl Microbiol Biotechnol 59: 15-32. doi: 10.1007/s00253-002-0975-y
    [3] Waschkowitz T, Rockstroh S, Daniel R (2009) Isolation and characterization of metalloproteases with a novel domain structure by construction and screening of metagenomic libraries. Appl Environ Microbiol 75: 2506-2516. doi: 10.1128/AEM.02136-08
    [4] Razzaq A, Shamsi S, Ali A, et al. (2019) Microbial proteases applications. Front Bioeng Biotechnol 7: 110. doi: 10.3389/fbioe.2019.00110
    [5] Zhu D, Wu Q, Hua L (2019) Industrial enzymes. Comprehensive Biotechnology Oxford: Pergamon, 1-13.
    [6] Graves PR, Haystead TAJ (2002) Molecular biologist's guide to proteomics. Microbiol Mol Biol Rev 66: 39-63. doi: 10.1128/MMBR.66.1.39-63.2002
    [7] Białkowska AM, Morawski K, Florczak T (2017) Extremophilic proteases as novel and efficient tools in short peptide synthesis. J Ind Microbiol Biotechnol 44: 1325-1342. doi: 10.1007/s10295-017-1961-9
    [8] Yang H, Li YC, Zhao MZ, et al. (2019) Precision de novo peptide sequencing using mirror proteases of Ac-LysargiNase and trypsin for large-scale proteomics. Mol Cell Proteomics 18: 773-785. doi: 10.1074/mcp.TIR118.000918
    [9] Theron LW, Divol B (2014) Microbial aspartic proteases: current and potential applications in industry. Appl Microbiol Biotechnol 98: 8853-8868. doi: 10.1007/s00253-014-6035-6
    [10] Eun HM (1996) 6-DNA Polymerases. Enzymology Primer for Recombinant DNA Technology San Diego: Academic Press, 345-489. doi: 10.1016/B978-012243740-3/50009-0
    [11] Olajuyigbe FM, Falade AM (2014) Purification and partial characterization of serine alkaline metalloprotease from Bacillus brevis MWB-01. Bioresour Bioprocess 1: 8. doi: 10.1186/s40643-014-0008-6
    [12] Cui H, Yang M, Wang L, et al. (2015) Identification of a new marine bacterial strain SD8 and optimization of its culture conditions for producing alkaline protease. PLOS One 10: e0146067. doi: 10.1371/journal.pone.0146067
    [13] Martínez-Medina GA, Barragán AP, Ruiz HA, et al. (2019) Fungal Proteases and Production of Bioactive Peptides for the Food Industry. Enzymes in Food Biotechnology Cambridge: Academic Press, 221-246. doi: 10.1016/B978-0-12-813280-7.00014-1
    [14] Tacon AGJ (2020) Trends in global aquaculture and aquafeed production: 2000–2017. Rev Fish Sci Aquacult 28: 43-56. doi: 10.1080/23308249.2019.1649634
    [15] Hossain TJ, Chowdhury SI, Mozumder HA, et al. (2020) Hydrolytic exoenzymes produced by bacteria isolated and identified from the gastrointestinal tract of Bombay duck. Front Microbiol 11. doi: 10.3389/fmicb.2020.02097
    [16] Selim KM, Reda RM (2015) Improvement of immunity and disease resistance in the Nile tilapia, Oreochromis niloticus, by dietary supplementation with Bacillus amyloliquefaciens. Fish Shellfish Immunol 44: 496-503. doi: 10.1016/j.fsi.2015.03.004
    [17] Su H, Xiao Z, Yu K, et al. (2020) Diversity of cultivable protease-producing bacteria and their extracellular proteases associated to scleractinian corals. PeerJ 8: e9055. doi: 10.7717/peerj.9055
    [18] Amin M (2018) Marine protease-producing bacterium and its potential use as an abalone probiont. Aquacult Rep 12: 30-35. doi: 10.1016/j.aqrep.2018.09.004
    [19] Maas RM, Deng Y, Dersjant-Li Y, et al. (2021) Exogenous enzymes and probiotics alter digestion kinetics, volatile fatty acid content and microbial interactions in the gut of Nile tilapia. Sci Rep 11: 8221. doi: 10.1038/s41598-021-87408-3
    [20] Anshary H, Kurniawan RA, Sriwulan S, et al. (2014) Isolation and molecular identification of the etiological agents of streptococcosis in Nile tilapia (Oreochromis niloticus) cultured in net cages in Lake Sentani, Papua, Indonesia. SpringerPlus 3: 627. doi: 10.1186/2193-1801-3-627
    [21] Champneys T, Castaldo G, Consuegra S, et al.Density-dependent changes in neophobia and stress-coping styles in the world's oldest farmed fish. R Soc Open Sci 5: 181473. doi: 10.1098/rsos.181473
    [22] Njiru M, Okeyo-Owuor J, Muchiri M, et al. (2004) Shifts in the food of Nile tilapia, Oreochromis niloticus (L.) in Lake Victoria, Kenya. Afr J Ecol 42: 163-170. doi: 10.1111/j.1365-2028.2004.00503.x
    [23] Moyle PB, Cech JJ (2004)  Fishes: An Introduction to Ichthyology New Jersey: Pearson Prentice Hall, 559.
    [24] BPM BPM Research Group, Bacteriological Growth Media: Composition, Preparation and Preservation of Nutritional Media for Culturing Bacteria, 2020 (2020) .Available from: https://sites.google.com/view/bpm-research-group/research/media-composition.
    [25] Hossain TJ, Alam MK, Sikdar D (2011) Chemical and microbiological quality assessment of raw and processed liquid market milks of Bangladesh. Cont J Food Sci Technol 5: 6-17.
    [26] Carter GR (1990) Isolation and identification of bacteria from clinical specimens. Diagnostic procedure in veterinary bacteriology and mycology Elsevier, 19-39. doi: 10.1016/B978-0-12-161775-2.50008-6
    [27] Zhang Z, Schwartz S, Wagner L, et al. (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7: 203-214. doi: 10.1089/10665270050081478
    [28] Wang Q, Garrity GM, Tiedje JM, et al. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267. doi: 10.1128/AEM.00062-07
    [29] Pruesse E, Peplies J, Glöckner FO (2012) SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829. doi: 10.1093/bioinformatics/bts252
    [30] Hossain TJ, Manabe S, Ito Y, et al. (2018) Enrichment and characterization of a bacterial mixture capable of utilizing C-mannosyl tryptophan as a carbon source. Glycoconjugate J 35: 165-176. doi: 10.1007/s10719-017-9807-2
    [31] Schoch CL, Ciufo S, Domrachev M, et al. (2020) NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford) 2020: baaa062. doi: 10.1093/database/baaa062
    [32] Ali Ferdausi, Das Sharup, Hossain Tanim Jabid, et al. (2021) Production optimization, stability, and oil emulsifying potential of biosurfactants from selected bacteria isolated from oil contaminated sites. R Soc Open Sci 8.
    [33] Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797. doi: 10.1093/nar/gkh340
    [34] Kumar S, Stecher G, Li M, et al. (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547-1549. doi: 10.1093/molbev/msy096
    [35] (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67: 1613-1617.
    [36] Hasegawa M, Kishino H, Saitou N (1991) On the maximum likelihood method in molecular phylogenetics. J Mol Evol 32: 443-445. doi: 10.1007/BF02101285
    [37] Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512-526.
    [38] Garrity GM, Bell JA, Lilburn TG (2004) Taxonomic outline of the prokaryotes. Bergey's manual of systematic bacteriology New York: Springer-Verlag.
    [39] Reda RM, Selim KM, El-Sayed HM, et al. (2018) In vitro selection and identification of potential probiotics isolated from the gastrointestinal tract of nile tilapia, Oreochromis niloticusProbiotics Antimicrob Proteins 10: 692-703. doi: 10.1007/s12602-017-9314-6
    [40] Bairagi A, Ghosh KS, Sen SK, et al. (2002) Enzyme producing bacterial flora isolated from fish digestive tracts. Aquacult Int 10: 109-121. doi: 10.1023/A:1021355406412
    [41] Kar N, Ghosh K (2008) Enzyme producing bacteria in the gastrointestinal tracts of Labeo rohita (Hamilton) and Channa punctatus (Bloch). Turkish J Fish Aquat Sci 8: 115-120.
    [42] Molinari L, Scoaris D, Pedroso R, et al. (2003) Bacterial microflora in the gastrointestinal tract of Nile tilapia, Oreochromis niloticus, cultured in a semi-intensive system. Acta Sci Biol Sci 25: 267-271.
    [43] Saha S, Roy RN, Sen SK, et al. (2006) Characterization of cellulase-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, Ctenopharyngodon idella (Valenciennes). Aquacult Res 37: 380-388. doi: 10.1111/j.1365-2109.2006.01442.x
    [44] Wu F, Chen B, Liu S, et al. (2020) Effects of woody forages on biodiversity and bioactivity of aerobic culturable gut bacteria of tilapia (Oreochromis niloticus). PLOS One 15: e0235560. doi: 10.1371/journal.pone.0235560
    [45] Haygood AM, Jha R (2018) Strategies to modulate the intestinal microbiota of Tilapia (Oreochromis sp.) in aquaculture: a review. Rev Aquacult 10: 320-333. doi: 10.1111/raq.12162
    [46] Afrilasari W, Widanarni, Meryandini A (2016) Effect of probiotic Bacillus megaterium PTB 1.4 on the population of intestinal microflora, digestive enzyme activity and the growth of catfish (Clarias sp.). HAYATI J Biosci 23: 168-172. doi: 10.1016/j.hjb.2016.12.005
    [47] Zorriehzahra MJ, Delshad ST, Adel M, et al. (2016) Probiotics as beneficial microbes in aquaculture: an update on their multiple modes of action: a review. Null 36: 228-241.
    [48] Yang C, Jiang M, Lu X, et al. (2021) Effects of dietary protein level on the gut microbiome and nutrient metabolism in tilapia (Oreochromis niloticus). Animals 11: 1024. doi: 10.3390/ani11041024
    [49] Zaky MMM, Ibrahim ME (2017) Screening of bacterial and fungal biota associated with Oreochromis niloticus in Lake Manzala and its impact on human health. Health 9: 697-714. doi: 10.4236/health.2017.94050
    [50] Boari CA, Pereira GI, Valeriano C, et al. (2008) Bacterial ecology of tilapia fresh fillets and some factors that can influence their microbial quality. Food Sci Technol 28: 863-867. doi: 10.1590/S0101-20612008000400015
    [51] Biedendieck R, Knuuti T, Moore SJ, et al. (2021) The “beauty in the beast”—the multiple uses of Priestia megaterium in biotechnology. Appl Microbiol Biotechnol 105: 5719-5737. doi: 10.1007/s00253-021-11424-6
    [52] Nicodème M, Grill JP, Humbert G, et al. (2005) Extracellular protease activity of different Pseudomonas strains: dependence of proteolytic activity on culture conditions. J Appl Microbiol 99: 641-648. doi: 10.1111/j.1365-2672.2005.02634.x
    [53] Asker MMS, Mahmoud MG, El Shebwy K, et al. (2013) Purification and characterization of two thermostable protease fractions from Bacillus megateriumJ Genet Eng Biotechnol 11: 103-109. doi: 10.1016/j.jgeb.2013.08.001
    [54] Ray AK, Roy T, Mondal S, et al. (2010) Identification of gut-associated amylase, cellulase and protease-producing bacteria in three species of Indian major carps. Aquacult Res 41: 1462-1469.
    [55] Lee MA, Liu Y (2000) Sequencing and characterization of a novel serine metalloprotease from Burkholderia pseudomalleiFEMS Microbiol Lett 192: 67-72. doi: 10.1111/j.1574-6968.2000.tb09360.x
    [56] Miyaji T, Otta Y, Shibata T, et al. (2005) Purification and characterization of extracellular alkaline serine protease from Stenotrophomonas maltophilia strain S-1. Lett Appl Microbiol 41: 253-257. doi: 10.1111/j.1472-765X.2005.01750.x
    [57] Bhowmik T, Marth EH (1988) Protease and peptidase activity of Micrococcus species. J Dairy Sci 71: 2358-2365. doi: 10.3168/jds.S0022-0302(88)79819-7
    [58] Rodarte MP, Dias DR, Vilela DM, et al. (2011) Proteolytic activities of bacteria, yeasts and filamentous fungi isolated from coffee fruit (Coffea arabica L.). Acta Sci Agron 33: 457-464.
    [59] Zeng A, Tan K, Gong P, et al. (2020) Correlation of microbiota in the gut of fish species and water. 3 Biotech 10: 472. doi: 10.1007/s13205-020-02461-5
    [60] Kim PS, Shin NR, Lee JB, et al. (2021) Host habitat is the major determinant of the gut microbiome of fish. Microbiome 9: 166. doi: 10.1186/s40168-021-01113-x
    [61] Liu H, Guo X, Gooneratne R, et al. (2016) The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci Rep 6: 24340. doi: 10.1038/srep24340
    [62] Burtseva O, Kublanovskaya A, Fedorenko T, et al. (2021) Gut microbiome of the White Sea fish revealed by 16S rRNA metabarcoding. Aquaculture 533: 736175. doi: 10.1016/j.aquaculture.2020.736175
    [63] Egerton S, Culloty S, Whooley J, et al. (2018) The gut microbiota of marine fish. Front Microbiol 9. doi: 10.3389/fmicb.2018.00873
    [64] Bereded N, Curto M, Domig K, et al. (2020) Metabarcoding analyses of gut microbiota of Nile tilapia (Oreochromis niloticus) from Lake Awassa and Lake Chamo, Ethiopia. Microorganisms 8: 1040. doi: 10.3390/microorganisms8071040
    [65] Hassaan MS, Mohammady EY, Soaudy MR, et al. (2021) Synergistic effects of Bacillus pumilus and exogenous protease on Nile tilapia (Oreochromis niloticus) growth, gut microbes, immune response and gene expression fed plant protein diet. Anim Feed Sci Technol 275: 114892. doi: 10.1016/j.anifeedsci.2021.114892
    [66] Wang M, Liu G, Lu M, et al. (2017) Effect of Bacillus cereus as a water or feed additive on the gut microbiota and immunological parameters of Nile tilapia. Aquacult Res 48: 3163-3173. doi: 10.1111/are.13146
    [67] Xia Y, Wang M, Gao F, et al. (2020) Effects of dietary probiotic supplementation on the growth, gut health and disease resistance of juvenile Nile tilapia (Oreochromis niloticus). Anim Nutr 6: 69-79. doi: 10.1016/j.aninu.2019.07.002
    [68] Giatsis C, Sipkema D, Smidt H, et al. (2015) The impact of rearing environment on the development of gut microbiota in tilapia larvae. Sci Rep 5: 18206. doi: 10.1038/srep18206
    [69] Bereded NK, Abebe GB, Fanta SW, et al. (2021) The Impact of sampling season and catching site (wild and aquaculture) on gut microbiota composition and diversity of Nile tilapia (Oreochromis niloticus). Biology (Basel) 10: 180.
    [70] Jaouadi NZ, Rekik H, Badis A, et al. (2013) Biochemical and molecular characterization of a serine keratinase from Brevibacillus brevis US575 with promising keratin-biodegradation and hide-dehairing activities. PLOS One 8: e76722. doi: 10.1371/journal.pone.0076722
    [71] Li HJ, Tang BL, Shao X, et al. (2016) Characterization of a New S8 serine protease from marine sedimentary photobacterium sp. A5–7 and the function of its protease-associated domain. Front Microbiol 7: 2016.
    [72] Saggu SK, Jha G, Mishra PC (2019) Enzymatic degradation of biofilm by metalloprotease from Microbacterium sp. SKS10. Front Bioeng Biotechnol 7: 192. doi: 10.3389/fbioe.2019.00192
    [73] Zhou C, Qin H, Chen X, et al. (2018) A novel alkaline protease from alkaliphilic Idiomarina sp. C9-1 with potential application for eco-friendly enzymatic dehairing in the leather industry. Sci Rep 8: 16467. doi: 10.1038/s41598-018-34416-5
    [74] Yildirim V, Baltaci MO, Ozgencli I, et al. (2017) Purification and biochemical characterization of a novel thermostable serine alkaline protease from Aeribacillus pallidus C10: a potential additive for detergents. J Enzyme Inhib Med Chem 32: 468-477. doi: 10.1080/14756366.2016.1261131
    [75] Chellappan S, Jasmin C, Basheer SM, et al. (2011) Characterization of an extracellular alkaline serine protease from marine Engyodontium album BTMFS10. J Ind Microbiol Biotechnol 38: 743-752. doi: 10.1007/s10295-010-0914-3
    [76] Niyonzima FN, More SS (2015) Purification and characterization of detergent-compatible protease from Aspergillus terreus gr. 3 Biotech 5: 61-70. doi: 10.1007/s13205-014-0200-6
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