Comparative analyses of gut microbiota reveal ammonia detoxification and nitrogen assimilation in Cyprinus carpio var. specularis
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, srovnávací studie
PubMed
38367166
DOI
10.1007/s12223-024-01151-6
PII: 10.1007/s12223-024-01151-6
Knihovny.cz E-zdroje
- Klíčová slova
- Cyprinus carpio, Fish, Foregut, Gut microbiome, Hindgut, Nitrogen assimilation,
- MeSH
- amoniak * metabolismus MeSH
- Bacteria * klasifikace metabolismus genetika izolace a purifikace MeSH
- dusík * metabolismus MeSH
- fylogeneze MeSH
- gastrointestinální trakt mikrobiologie metabolismus MeSH
- kapři * mikrobiologie metabolismus MeSH
- metabolická inaktivace MeSH
- metabolické sítě a dráhy MeSH
- RNA ribozomální 16S genetika MeSH
- střevní mikroflóra * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- srovnávací studie MeSH
- Názvy látek
- amoniak * MeSH
- dusík * MeSH
- RNA ribozomální 16S MeSH
The complex niche of fish gut is often characterized by the associated microorganisms that have implications in fish gut-health nexus. Although efforts to distinguish the microbial communities have highlighted their disparate structure along the gut length, remarkably little information is available about their distinct structural and functional profiles in different gut compartments in different fish species. Here, we performed comparative taxonomic and predictive functional analyses of the foregut and hindgut microbiota in an omnivorous freshwater fish species, Cyprinus carpio var. specularis, commonly known as mirror carp. Our analyses showed that the hindgut microbiota could be distinguished from foregut based on the abundance of ammonia-oxidizing, denitrifying, and nitrogen-fixing commensals of families such as Rhodospirillaceae, Oxalobacteraceae, Nitrosomonadaceae, and Nitrospiraceae. Functionally, unique metabolic pathways such as degradation of lignin, 2-nitrobenzoate, vanillin, vanillate, and toluene predicted within hindgut also hinted at the ability of hindgut microbiota for assimilation of nitrogen and detoxification of ammonia. The study highlights a major role of hindgut microbiota in assimilating nitrogen, which remains to be one of the limiting nutrients within the gut of mirror carp.
Department of Zoology Deshbandhu College Kalkaji New Delhi 110019 India
Fish Molecular Biology Laboratory Department of Zoology University of Delhi Delhi 110007 India
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Arora PK, Sharma A (2015) New metabolic pathway for degradation of 2-nitrobenzoate by Arthrobacter sp. SPG. Front Microbiol 6551
Baldani JI, Rouws L, Cruz LM, Olivares FL, Schmid M, Hartmann A (2014) The family Oxalobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg, Germany, pp 919–974 DOI
Banerjee G, Ray AK (2017) Bacterial symbiosis in the fish gut and its role in health and metabolism. Symbiosis 72:1–11 DOI
Baskaran V, Patil PK, Antony ML, Avunje S, Nagaraju VT, Ghate SD, Nathamuni S, Dineshkumar N, Alavandi SV, Vijayan KK (2020) Microbial community profiling of ammonia and nitrite oxidizing bacterial enrichments from brackishwater ecosystems for mitigating nitrogen species. Sci Rep 10:5201 PubMed DOI PMC
Bauer MA, Kainz K, Carmona-Gutierrez D, Madeo F (2018) Microbial wars: competition in ecological niches and within the microbiome. Microb Cell 5:215–219 PubMed DOI PMC
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300 DOI
Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857 PubMed DOI PMC
Bucking C, Wood CM (2012) Digestion of a single meal affects gene expression of ion and ammonia transporters and glutamine synthetase activity in the gastrointestinal tract of freshwater rainbow trout. J Comp Physiol B 182:341–350 PubMed DOI
Butt RL, Volkoff H (2019) Gut microbiota and energy homeostasis in fish. Front Endocrinol 10:9 DOI
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583 PubMed DOI PMC
Chu BC, Garcia-Herrero A, Johanson TH, Krewulak KD, Lau CK, Peacock RS, Slavinskaya Z, Vogel HJ (2010) Siderophore uptake in bacteria and the battle for iron with the host; a bird’s eye view. Biometals 23:601–611 PubMed DOI
Daims H, Wagner M (2018) Nitrospira. Trends Microbiol 26462–463
Daims H (2014) The family Nitrospiraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg, Germany, pp 733–749 DOI
Das P, Babaei P, Nielsen J (2019) Metagenomic analysis of microbe-mediated vitamin metabolism in the human gut microbiome. BMC Genom 20:208 DOI
de Bruijn I, Liu Y, Wiegertjes GF, Raaijmakers JM (2018) Exploring fish microbial communities to mitigate emerging diseases in aquaculture. FEMS Microbiol Ecol 94:fix161 DOI
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072 PubMed DOI PMC
Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN et al (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688 PubMed DOI PMC
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461 PubMed DOI
Egerton S, Culloty S, Whooley J, Stanton C, Ross RP (2018) The gut microbiota of marine fish. Front Microbiol 9:873 PubMed DOI PMC
Ellermann M, Arthur JC (2017) Siderophore-mediated iron acquisition and modulation of host-bacterial interactions. Free Radic Biol Med 105:68–78 PubMed DOI
Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I Accuracy Assessment Genome Res 8:175–185 PubMed
Fukami J, Cerezini P, Hungria M (2018) Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express 8:73 PubMed DOI PMC
Gonçalves AT, Gallardo-Escárate C (2017) Microbiome dynamic modulation through functional diets based on pre- and probiotics (mannan-oligosaccharides and Saccharomyces cerevisiae) in juvenile rainbow trout (Oncorhynchus mykiss). J Appl Microbiol 122:1333–1347 PubMed DOI
Görgényi J, Boros G, Vitál Z, Mozsár A, Várbíró G, Vasas G, Borics G (2016) The role of filter-feeding Asian carps in algal dispersion. Hydrobiologia 764:115–126 DOI
Han M, Yang K, Yang P, Zhong C, Chen C, Wang S, Lu Q, Ning K (2020) Stratification of athletes’ gut microbiota: the multifaceted hubs associated with dietary factors, physical characteristics and performance. Gut Microbes 12:1842991
Hira P, Bajaj A, Puri A, Talwar C et al (2019) Microbial genomics and metagenomics in India: explorations and perspectives. Proc Indian National Sci Acad 85:999–1023
Holmes AJ, Yi YV, Colakoglu F, Cliff JB, Klaassens E et al (2017) Diet-microbiome interactions in health are controlled by intestinal nitrogen source constraints. Cell Metab 25:140–151 PubMed DOI
Ikeda-Ohtsubo W, Brugman S, Warden CH, Rebel JMJ, Folkerts G, Pieterse CMJ (2018) How can we define “Optimal Microbiota?”: a comparative review of structure and functions of microbiota of animals, fish, and plants in agriculture. Front Nutr 5:90 PubMed DOI PMC
Irazoki O, Hernandez SB, Cava F (2019) Peptidoglycan muropeptides: release, perception, and functions as signaling molecules. Front Microbiol 10:500 PubMed DOI PMC
Jami M, Ghanbari M, Kneifel W, Domig KJ (2015) Phylogenetic diversity and biological activity of culturable Actinobacteria isolated from freshwater fish gut microbiota. Microbiol Res 175:6–15 PubMed DOI
Kolde R, Kolde MR (2015) Package ‘pheatmap’. R package 1:790. https://cran.rproject.org/web/packages/pheatmap/pheatmap.pdf
Kreuzer M, Heindl U, Roth-Maier DA, Kirchgessner M (1991) Cellulose fermentation capacity of the hindgut and nitrogen turnover in the hindgut of sows as evaluated by oral and intracecal supply of purified cellulose. Arch Anim Nutr 41:359–372
Ktari N, Jridi M, Bkhairia I, Sayari N, Ben Salah R, Nasri M (2012) Functionalities and antioxidant properties of protein hydrolysates from muscle of zebra blenny (Salaria basilisca) obtained with different crude protease extracts. Food Res Intl 49:747–756 DOI
Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R (2011) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Bioinformatics 10:10
Kulichevskaya IS, Naumoff DG, Miroshnikov KK, Ivanova AA et al (2020) Limnoglobus roseus gen. nov., sp. nov., a novel freshwater planctomycete with a giant genome from the family Gemmataceae. Intl J Syst Evol Microbiol 70:1240–1249 DOI
Kulichevskaya IS, Serkebaeva YM, Kim Y, Rijpstra WIC, Damsté JSS, Liesack W, Dedysh SN (2012) Telmatocola sphagniphila gen. nov., sp. nov., a novel dendriform planctomycete from northern wetlands. Front Microbiol 3:146 PubMed DOI PMC
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874 PubMed DOI PMC
Le MH, Wang D (2020) Structure and membership of gut microbial communities in multiple fish cryptic species under potential migratory effects. Sci Rep 10:7547 PubMed DOI PMC
Le HT, Shao X, Krogdahl Å, Kortner TM, Lein I, Kousoulaki K, Lie KK, Sæle Ø (2019) Intestinal function of the stomachless fish, Ballan Wrasse (Labrus bergylta). Front Mar Sci 6:140 DOI
Leahy JG, Olsen RH (1997) Kinetics of toluene degradation by toluene-oxidizing bacteria as a function of oxygen concentration, and the effect of nitrate. FEMS Microbiol Ecol 23:23–30 DOI
Lee C, Park C (2017) Bacterial responses to glyoxal and methylglyoxal: reactive electrophilic species. Int J Mol Sci 18:E169 DOI
Lewin WC, Kamjunke N, Mehner T (2003) Phosphorus uptake by Microcystis during passage through fish guts. Limnol Oceanogr 48:2392–2396 DOI
Li XM, Zhu YJ, Yan QY, Ringø E, Yang DG (2014) Do the intestinal microbiotas differ between paddlefish (Polyodon spathala) and bighead carp (Aristichthys nobilis) reared in the same pond. J Appl Microbiol 117:1245–1252 PubMed DOI
Liu H, Guo X, Gooneratne R, Lai R, Zeng C, Zhan F, Wang W (2016) The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci Rep 6:24340 PubMed DOI PMC
Llewellyn MS, Boutin S, Hoseinifar SH, Derome N (2014) Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries. Front Microbiol 5:207 PubMed DOI PMC
Madigan M, Cox SS, Stegeman RA (1984) Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae. J Bacteriol 157:73–78 PubMed DOI PMC
McDonald R, Zhang F, Watts JE, Schreier HJ (2015) Nitrogenase diversity and activity in the gastrointestinal tract of the wood-eating catfish Panaque nigrolineatus. ISME J 9:2712–2724 PubMed DOI PMC
McIlroy SJ, Nielsen PH (2014) The family Saprospiraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg, Germany, pp 863–889 DOI
McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531 PubMed DOI PMC
Mitchell AM, Srikumar T, Silhavy TJ (2018) Cyclic Enterobacterial common antigen maintains the outer membrane permeability barrier of Escherichia coli in a manner controlled by YhdP. Mbio 9:e01321-e1418 PubMed DOI PMC
Nagar S, Talwar C, Bharti M, Yadav S, Siwach S, Negi RK (2021) Metagenome-assembled genomes recovered from the datasets of a high-altitude Himalayan hot spring Khirganga, Himachal Pradesh. India DIB 39:107551
Nagar S, Bharti M, Negi RK (2023) Genome-resolved metagenomics revealed metal-resistance, geochemical cycles in a Himalayan hot spring. Appl Microbiol Biotechnol 107:3273–3289 PubMed DOI
Nielsen S, Walburn JW, Vergés A, Thomas T, Egan S (2017) Microbiome patterns across the gastrointestinal tract of the rabbitfish Siganus fuscescens. PeerJ 5:e3317 PubMed DOI PMC
Ohkuma M, Noda S, Kudo T (1999) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65:4926–4934 PubMed DOI PMC
Oren A, Xu XW (2014) The family Hyphomicrobiaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg, Germany, pp 247–281
Parata L, Nielsen S, Xing X, Thomas T, Egan S, Vergés A (2020) Age, gut location and diet impact the gut microbiome of a tropical herbivorous surgeonfish. FEMS Microbiol Ecol 96:fiz179 PubMed
Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26:715–721 PubMed DOI
Perna S, Alalwan TA, Alaali Z, Alnashaba T, Gasparri C et al (2019) The role of glutamine in the complex interaction between gut microbiota and health: a narrative review. Intl J Mol Sci 20:5232 DOI
Perry WB, Lindsay E, Payne CJ, Brodie C, Kazlauskaite R (2020) The role of the gut microbiome in sustainable teleost aquaculture. Proc Royal Soc B 287:20200184 DOI
Prosser JI, Head IM, Stein LY (2014) The family Nitrosomonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg, Germany, pp 901–918 DOI
Pujalte MJ, Lucena T, Ruvira MA, Arahal DR, Macián MC (2014) The family Rhodobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg, Germany, pp 439–512 DOI
Rahman MM (2015) Effects of co-cultured common carp on nutrients and food web dynamics in rohu aquaculture ponds. Aquac Environ Interact 6:223–232 DOI
Ramos-Molina B, Queipo-Ortuño MI, Lambertos A, Tinahones FJ, Peñafiel R (2019) Dietary and gut microbiota polyamines in obesity- and age-related diseases. Front Nutr 6:24 PubMed DOI PMC
Ravin NV, Rakitin AL, Ivanova AA, Beletsky AV, Kulichevskaya IS, Mardanov AV, Dedysh SN (2018) Genome analysis of Fimbriiglobus ruber SP5 DOI
Reese AT, Pereira FC, Schintlmeister A, Berry D et al (2018) Microbial nitrogen limitation in the mammalian large intestine. Nat Microbiol 3:1441–1450 PubMed DOI PMC
Rekdal VM, Bernadino PN, Luescher MU et al (2020) A widely distributed metalloenzyme class enables gut microbial metabolism of host- and diet-derived catechols. Elife 9:e50845 DOI
Ringø E, Zhou Z, Vecino J, Wadsworth S, Romero J et al (2016) Effect of dietary components on the gut microbiota of aquatic animals. Aquac Nutr 22:219–282 DOI
Sabree ZL, Moran NA (2014) Host-specific assemblages typify gut microbial communities of related insect species. Springerplus 3:138 PubMed DOI PMC
Shannon P, Markiel A, Ozier O, Baliga NS et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504 PubMed DOI PMC
Smith LS (1980) Digestion in teleost fishes. Fish feeds technology AO/UNDP Aquaculture Development and Coordination Programme Rome 3–18
Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506 PubMed DOI
Sullam KE, Essinger SD, Lozupone CA, O’Connor MP et al (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21:3363–3378 PubMed DOI
Talwar C, Nagar S, Lal R, Negi RK (2018) Fish gut microbiome: current approaches and future perspectives. Indian J Microbiol 58:397–414 PubMed DOI PMC
Talwar C, Singh AK, Choksket S, Korpole S, Lal R, Negi RK (2020) Salinicoccus cyprini sp. nov., isolated from the gut of mirror carp, Cyprinus carpio var. specularis. Intl J Sys Evol Microbiol 70:4111–4118 DOI
Wang AR, Ran C, Ringø E, Zhou ZG (2018) Progress in fish gastrointestinal microbiota research. Rev Aquac 10:626–640 DOI
Weber MJ, Brown ML (2011) Relationships among invasive common carp, native fishes, and physicochemical characteristics in upper Midwest (USA) lakes. Ecol Freshw Fish 20:270–278 DOI
Xu Z, Lei P, Zhai R, Wen Z, Jin M (2019) Recent advances in lignin valorization with bacterial cultures: microorganisms, metabolic pathways, and bio-products. Biotechnol Biofuels 12:32 PubMed DOI PMC
Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand JD, Kempher ML, Wu L, Wang Y, Liao L, Li X (2016) Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ Microbiol 12:4739–4754
Ye L, Amberg J, Chapman D, Gaikowski M, Liu WT (2014) Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. ISME J 8:541–551 PubMed DOI
Yu H, Guo Z, Shen S, Shan W (2016) Effects of taurine on gut microbiota and metabolism in mice. Amino Acids 48:1601–1617 PubMed DOI
Zeng A, Tan K, Gong P, Lei P, Guo Z (2020) Correlation of microbiota in the gut of fish species and water. 3 Biotech 10:472 PubMed DOI PMC