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Siddiqui, R.;  Soopramanien, M.;  Alharbi, A.M.;  Alfahemi, H.;  Khan, N.A. Importance of the Gut Microbiome. Encyclopedia. Available online: https://encyclopedia.pub/entry/26596 (accessed on 20 June 2024).
Siddiqui R,  Soopramanien M,  Alharbi AM,  Alfahemi H,  Khan NA. Importance of the Gut Microbiome. Encyclopedia. Available at: https://encyclopedia.pub/entry/26596. Accessed June 20, 2024.
Siddiqui, Ruqaiyyah, Morhanavallee Soopramanien, Ahmad M. Alharbi, Hasan Alfahemi, Naveed Ahmed Khan. "Importance of the Gut Microbiome" Encyclopedia, https://encyclopedia.pub/entry/26596 (accessed June 20, 2024).
Siddiqui, R.,  Soopramanien, M.,  Alharbi, A.M.,  Alfahemi, H., & Khan, N.A. (2022, August 29). Importance of the Gut Microbiome. In Encyclopedia. https://encyclopedia.pub/entry/26596
Siddiqui, Ruqaiyyah, et al. "Importance of the Gut Microbiome." Encyclopedia. Web. 29 August, 2022.
Importance of the Gut Microbiome
Edit

“Microbiome” refers to microorganisms inhabiting multicellular organisms, from animals to plants. The microbiome is made up of bacteria, archaea, protists, fungi, and viruses. An overview of several species whose gut microbiota have been evaluated.

gut microbiota fish animal Birds Reptiles Invertebrates Amphibians

1. Fish

Fish are thought to be among the most successful anamniotic ectotherms that reside in marine and freshwater habitats, and can adapt to live in some of the most extreme environments, such as those rich in hydrogen sulfide [1]. Although fish represent a vast taxonomic and ecologically diverse category, the comprehension of their gut microflora is only beginning to come to light, revealing low phylogenetic diversity, with ProteobacteriaFirmicutes, and Bacteroidetes representing approximately 90% of the fish intestinal microbiota. [2] Previously, a study investigated the antibacterial effects of the strains using antibacterial disc diffusion assays; Bacillus sp. PRV3 and Bacillus sp. PRV23, isolated from the gut of fish in Kerala, India; Oreochromis mossambicus (tilapia), Hypselo barbuskolus (koora), and Punitus melanampyx (kudukonda), and the herbivorous fish; Nemacheilus menoni (ayira) and Channa murulius (cherumeen). The results showed that fish bacterial metabolites were able to inhibit the activities of several pathogenic bacteria, namely KlebsiellaS. aureusEscherichia coliProteus mirabilisSerratia marcescensVibrio parahaemolyticus, and Vibrio cholorae [3]. Moreover, the gas chromatography–mass spectrometry results for the cell-free metabolite suspension revealed the presence of molecules with previously reported antimicrobial/antibacterial potentials, namely Neopentyl Glycol, Hentriacontane, Phenol, 2,4-Bis(1,1-Dimethylethyl, Heptacosane, and Methyl 3-(1-Pyrrolo)Thiophene-2, some of which were plant metabolites [4][5][6][7][8][9]. Of note, the study also reported that those bacteria inhabiting the gut of the fish produced secondary metabolites that reduced the viability of two cancer cells (HeLa and MCF-7), and furthermore, exhibited an apoptosis-like effect in cells post treatment [3].
Moreover, the antibacterial efficacies of metabolites produced by bacteria (E. coli, G-pos-bacilliS. aureusStaphylococcus auricularisAeromonas hydrophila, and G-neg-bacilli) isolated from the gut of tilapia fish (Oreochromis mossambicus) was assessed against the clinical isolates: Streptococcus pyogenes ATCC 49399, E. coli K1 MTCC 710859, P. aeruginosa ATCC 10145, methicillin-resistant S. aureus MTCC 381,123, and E. coli K-12 MTCC 817,356 (non-clinical isolate) via bactericidal assays investigating bacterial viability in comparison to controls (the antibiotic gentamicin and Roswell Park Memorial Institute (RPMI) media). The results revealed that the gut bacteria of tilapia exhibited bactericidal efficacy against P. aeruginosa and E. coli K1, while only S. aureus did not exhibit bactericidal activity against MRSA, S. auricularis and A. hydrophila, and Gram-negative-bacilli exhibited bactericidal activity against S. pyogenes [4]. In another study, Bacillus licheniformis (P40 strain) isolated from the intestines of teleost fish Leporinus sp. synthesized an antibacterial peptide that exhibited antibacterial activity against Bacillus cereusL. monocytogenes, and Streptococcus spp. [10].
Additionally, the lactic acid bacteria Lactobacillus sp. isolated from the gut of mullet fish (Mugil cephalus), were found to produce a 18kDa bacteriocin [11]Salmonella enterica subsp. enterica serovar Typhimurium ATCC 14,028 and Listeria monocytogenes ATCC 19,115 isolated from beluga (Huso huso) and Persian sturgeon (Acipenser persicus) have been reported to produce 5 and 3 kDa bacteriocins that exhibit antibacterial activity against A. hydrophilaE. coliS. aureusVibrio anguillarumListeria spp., Salmonella spp., and B. cereus [11]. In a study, the antibacterial potential of 27 bacteria isolated from the freshwater fish CatlaCyprinus carpio, Cirrhinus mirigala, and Labeo rohita were assessed, and the results showed that select bacteria caused growth inhibition of A. hydrophila [12]. Another study identified the antibacterial activity of secondary metabolites produced by Actinobacteria isolated from the gut of two fish species, Schizocypris altidorsalis and Schizothorax zarudnyi. Some of the isolates exhibited antibacterial effects against StreptomycesNocardiopsisMicromonospora, and Saccharomonospora species [13].

2. Reptiles

Extant non-avian reptiles are ectothermic amniotes and vertebrates that reside on every continent except Antarctica, and inhabit almost all biomes, including terrestrial, freshwater, and marine habitats, which may expose them to a variety of microorganisms, radiation, and/or heavy metals [14][15]. At present, there are limited studies on the gut microbiome composition of reptiles; however, with the availability of next-generation sequencing technologies, it has been revealed that the core gut microbiome of reptiles consists of ProteobacteriaFirmicutes, and Bacteroidetes, and that reptile gut bacterial communities are more comparable to those of birds than those of mammals [16]. Recently, the gut microbial compositions of four farmed snakes in China were elucidated [17]. The study revealed that the most abundant phyla were BacteroidetesProteobacteriaFirmicutesFusobacteria, and Actinobacteria. The authors hypothesized that the host species is a significant influence affecting gut microbiome diversity, and affirmed the need to investigate whether the immunity and growth of farmed snake populations may be augmented by inoculating fecal suspensions from healthy wild snakes [17]. Another study revealed the structure and distribution of gut bacteria in various parts of the gastrointestinal tract of the snake species Rhabdophis subminiatus [18]. Furthermore, a study examined 22 snakes of three different species from the Philippines and investigated whether the host ecology and species differences were correlated with differences in microbial diversity within the gut and mouth [19]. These three species reside in three varying habitats: marine, semi-arboreal, and arboreal. The data obtained were indicative that the microbial diversity of the gut microbiome was correlated with host ecological and phylogenetic differences [19].
Studies investigating the effects of gut microbial metabolites, however, are few and far between. Recently, studies were conducted to examine the efficacy of bacterial metabolites produced from the gut microbiota of the python, water monitor lizard, and turtle [4]. Antibacterial activities of metabolites produced by the gut bacteria (Citrobacter freundiiBacillus paramycoidesCitrobacter braakiiBacillus albusP. mirabilis, and Escherichia fergusonii) isolated from the gut of python (Malayopython reticulatus) were assessed using bactericidal assays. The results revealed that the metabolites from C. freundiiC. braakiiP. mirabilis, and E. fergusonii exhibited potent antibacterial activity against MRSA, while the metabolites from all bacteria except E. fergusonii exhibited antibacterial effects against S. pyogenes and P. aeruginosa [4]. Later, bacteria (Enterobacter cloacaeA. hydrophila, and P. aeruginosa) cultivated from the gut of Cuora amboinensis (turtle) were subjected to conditioned media (CM) preparation, which is a cell-free bacterial metabolite suspension. The overall results from the study demonstrated that the CM from the isolated bacteria exhibited antibacterial effects against various Gram-positive (B. cereus, methicillin-resistant S. aureus and S. pyogenes) and Gram-negative (Klebsiella pneumoniaeS. marcescensP. aeruginosaSalmonella enterica, and neuropathogenic E. coli K1) pathogenic bacteria [4].
In another very important study, a plethora of bacteria—C. freundiiA. hydrophilaE. coliS. aureusP. mirabilia, and Staphylococcus sp.—were isolated from the gut of a water monitor lizard (Varanus salvator) and were subjected to CM preparation [20]. The CM were tested for their antibacterial efficacy using bactericidal assays, and results revealed that CM from P. mirabilisE. coliStaphylococcus sp., and S. aureus exhibited antibacterial activity against B. cereus, while CM from C. freundiiA. hydrophilaE. coli, and Staphylococcus sp. exhibited antibacterial activity against MRSA. CM from E. coliC. freundiiStaphylococcus sp., and S. aureus revealed antibacterial efficacy against S. pyogenes, and CM from Proteus mirabilis, C. freundiiE. coliStaphylococcus sp., and S. aureus exhibited antibacterial activity against P. aeruginosa. Finally, CM from P. mirabilisA. hydrophilaC. freundiiE. coli, and Staphylococcus sp. exhibited antibacterial activity against S. enterica, and all CM exhibited antibacterial activity against K. pneumoniae and S. marcescens [20]. Furthermore, liquid chromatography–mass spectrometry (LC–MS) results revealed the presence of secondary metabolites with previously reported antibacterial activity alkaloids, flavonoids, terpenes, hydroxylated fatty acids, oxygenated fatty acids, and pyrazine derivative. The presence of Dehydrocurdione, a molecule responsible for the antibacterial effect of turmeric, was also noted [20][21].
Interestingly, in previous studies it was also shown that CM prepared from the gut bacteria of the crocodile (Crocodylus porosus), particularly Aeromonas dhakensisPseudomonas guezennei, and P. aeruginosa, exhibited potent effects against breast, cervical, and prostate cancer cell lines. LC–MS results further supported these findings, as this revealed the presence of molecules with reported anticancer activity in the active CM, namely PD 98,059 and L, L-Cyclo(leucylprolyl). Moreover, LC–MS revealed molecules with previously reported antibacterial activity in the active CM: lactic acid, F-Honaucin A, L, L-Cyclo(leucylprolyl), Granisetron metabolite 1, and Phenylethylamine, suggesting that those CM might also exhibit antibacterial potential [22]. Additionally, it was reported that lactic acid, F-Honaucin A, L, L-Cyclo(leucylprolyl), Granisetron metabolite 1, and Phenylethylamine exhibited anticancer activity against breast, cervical, and prostate cancer cell lines. Again, this was supported by LC–MS analysis, which showed molecules with reported anticancer activity in the active CM, namely C75, 3-Butylidene-7-hydroxyphthalide, Estrone 16-oxime, Enigmol, Proglumide, and S-Allyl-L-cysteine, and molecules with reported antibacterial activity, namely Benzocaine and Quindoxin [22]. However, the antibacterial effects of these CM need to be investigated in future studies.

3. Birds

Avian reptiles/birds are a diverse group of amniotic endothermic vertebrates with a global distribution, and many species undergo lengthy seasonal migrations across great distances [23][24]. Furthermore, a variety of diets and life history strategies are utilized by birds, and thus elucidating their microbiome is of interest [23][24]. The gut microbiome of birds is dominated by members of the Firmicutes, with ActinobacteriaBacteroidetes, and Proteobacteria, although the relative proportions of these is known to vary amongst different species [24].
Compared to other nonmammalian vertebrates, comprehension of the bird microbiome is greater; however, most avian microbiome reports have been focused on economically important species; for example, chicken and turkey [24]. In a study, the antimicrobial activity of cell-free supernatant (CFS) from Enterococcus faecium KQ 2.6 isolated from the fecal matter of Pavo cristatus (peacock) was assessed against a plethora of pathogenic bacteria: Bacillus subtilisB. cereusS. pyogenesS. aureusE. faecalisE. coliP. aeruginosaK. pneumoniaeSalmonella enterica sub. enterica serovar paratyphi, Staphylococcus epidermidisAspergillus niger, and Candida albicans. The results generated showed that the CFS prepared exhibited antibacterial activity against the selected bacteria [25]. The antibacterial potential of CM prepared from Escherichia fergusoniiShigella flexneriB. cereus, and E. faecalis isolated from the gastrointestinal tract of a wild Gallus gallus domesticus (Chicken) was assessed and the results indicated that all CM exhibited bactericidal efficacies against E. coli K1, S. pyogenes, and P. aeruginosa, while all CM except S. flexneri exhibited bactericidal effects against MRSA [4]. Moreover, researchers previously reported that B. cereus and Bacillus velezensis isolated from the fecal matter and gut of Columba livia domestica (pigeon) exhibited anticancer activity against cervical, breast, and prostate cancer cell lines, and exhibited cytotoxicity towards HeLa cervical cancer cells at IC50 concentration of 10.65 and 15.19 µg/mL. LC–MS results for the CM of these active bacteria showed the presence of molecules with reported anticancer (dihydroxymelphalan) and antibacterial activity (citric acid) [26].

4. Amphibians

Amphibians are ectothermic, tetrapod vertebrates that reside in a variety of habitats, living in terrestrial, arboreal, fossorial, or freshwater aquatic environments, and are amongst the world’s most vulnerable groups of animals, with 40% of these species in danger of extinction [27][28]. There is limited information regarding the gut microbiome of amphibians, and recently, a study was conducted that investigated the correlation between the diversity of diet and the gut microbiome of adult fire salamanders in Belgian forests, using high-throughput DNA metabarcoding [28]. It was shown that the diet composition was driven by sex, and this influenced the microbiome composition in the fire salamander. However, no correlation was observed between diet diversity and gut microbiome diversity. Another study revealed that the leopard frog gut bacterial communities underwent significant changes when going through metamorphosis [29].
Recently, the antibacterial properties of two bacteria, namely P. mirabilis and Proteus vulgaris, isolated from the American bull frog gut (Lithobates catesbeianus) were elucidated against several clinical isolates, namely E. coli K1 MTCC 710859, P. aeruginosa ATCC 10145, methicillin-resistant S. aureus MTCC 381123, S. pyogenes ATCC 49,399, and the non-clinical isolate of E. coli K-12 MTCC 817,356 [4]. Antibacterial activity was established via bactericidal assays conducted following the preparation of the metabolites from the two bacterial species. The results revealed that metabolites from both bacteria exhibited antibacterial effects against P. aeruginosa, E. coli K1, and S. pyogenes, while only P. vulgaris exhibited antibacterial activity against MSRA. Moreover, post heat inactivation, the metabolite suspension prepared from each bacterium retained their antibacterial activity, hinting that the active molecule(s) responsible for the antibacterial activity might not be proteinaceous in nature [4]. Thus, further studies must be conducted focusing on amphibian gut microbial metabolites as well as gut microbiome composition, with the aim of unveiling molecules with antibacterial potential to alleviate the burden of infectious diseases among humans, as well as for the conservation and health management of amphibians [30].

5. Invertebrates

Invertebrates are thought to constitute the majority of animal species, comprising an estimated 97% of all species on earth, and thus residing in a variety of ecosystems, such as deep in the ocean and in surface water, soil, and other terrestrial areas, including those with the most difficult conditions for biological life. Furthermore, their diet consists of a variety of food [31][32][33]. Although previously neglected by scientists, currently the most studied model organisms are invertebrates, namely Drosophila melanogaster and Caenorhabditis elegans [33]. Recently, studies have begun to explore the impact of the gut and its effects on ageing, using invertebrates as model organisms [33]. Despite the distinct differences between the invertebrate gut and the corresponding microbiome of mammalian models and humans, several comparisons in regard to gut dysbiosis, immune function, and intestinal decline can be made; thus, utilizing the gut microbiome of these abundant species for the benefit of human and animal health is warranted, given the key role these species play in the food web, as well as in organic matter decomposition [33].
The antibacterial potential of CM produced from the gut bacteria of the mud crab (Scylla serrata), red-headed centipede (Scolopendra subspinipes) and rose hair tarantula (Grammostola rosea) was assessed [4]Kluyvera georgianaLysinibacillus fusiformisP. aeruginosa, and Bacillus proteolyticus were isolated from the centipede, while S. aureusB. subtilisPseudomonas putida, and G-neg-bacilli were isolated from the tarantula, and Proteus alimentorumK. pneumoniae, and P. vulgaris isolated from the crab. The results showed that all CM from the centipede exhibited antibacterial activity against E. coli K1 and P. aeruginosa, apart from B. proteolyticus. Additionally, all CM exhibited antibacterial activity against S. pyogenes and MRSA. From the tarantula, all CM exhibited antibacterial activities against E. coli K1 and P. aeruginosa, besides the G-neg-bacilli; all CM exhibited antibacterial activity against S. pyogenes, and only CM from P. putida and G-neg-bacilli exhibited antibacterial efficacy against MRSA. From the crab, K. pneumoniae and P. vulgaris exhibited bactericidal efficacy against S. pyogenesE. coli K1, and P. aeruginosa, while none of the CM exhibited antibacterial effects against MRSA [4]. Another interesting study revealed that the larvae of Lucilia sericata or sheep blowfly, which are utilized in maggot debridement therapy, had potent antimicrobial effects [34].
Cockroaches are known to share ecological niches with humans and other animals, plausibly being exposed routinely to a variety of microorganisms in their habitats, and thus are of interest [35][36][37]. Previous studies revealed the potent antibacterial effects of extracts from various body organs of cockroaches (Periplaneta americana) against MRSA and neuropathogenic E. coli K1 [37]. More recently, the antibacterial potential of CM prepared from gut bacteria isolated from two species of cockroach was assessed. S. marcescens and E. coli were isolated from Gromphadorhina portentosa (Madagascar), while Klebsiella sp., Citrobacter sp., Bacillus sp., Klebsiella sp., and Streptococcus sp. were isolated from Blaptica dubia (Dubia) cockroach, and metabolite suspensions were prepared before elucidating the bactericidal properties [38]. The results showed that all CM exhibited antibacterial activity against B. cereus, while only CM from S. marcescens, E. coli, Klebsiella sp., and Citrobacter sp. exhibited antibacterial activity against MRSA, and all CM except Bacillus sp. exhibited antibacterial activity against S. pyogenes [38]. Moreover, the study revealed that CM from those cockroach species also exhibited anti-amoebic efficacy [38]. In another report, P. aeruginosa and B. subtilis isolated from the gut of Heterometrus spinifer (scorpion) depicted anticancer activity against cervical, breast, and prostate cancer cell lines. Through LC–MS, researchers also noted that those bacteria produced molecules with previously reported anticancer activity; 3-butylidene-7-hydroxyphthalide, U-0126, and proglumide. However, the LC–MS revealed that the active bacteria also produce molecules with reported antibacterial activities, namely dextromethorphan, citric acid, and 3-Butylidene-7-hydroxyphthalide [39].

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