A Metagenomic Study of Intestinal Microbial Diversity in Relation to Feeding Habits of Surface and Cave-Dwelling Sinocyclocheilus Species
Tóm tắt
Light is completely absent in cave habitats, causing a shortage or lack of autochthonous photosynthesis. Thus, understanding the mechanisms underlying the ability of organisms to adapt to the unique cave habitat is of great interest. We used high-throughput sequencing of the 16S ribosomal RNA gene of intestinal microorganisms from 11 Sinocyclocheilus (Cypriniformes: Cyprinidae) species, to explore the characteristics of intestinal microorganisms and the adaptive mechanisms of Sinocyclocheilus cavefish and surface fish. We found that the α-diversity and richness of the intestinal microbiome were much higher in cavefish than in surface fish. Principal coordinate analysis showed that cavefish and surface fish formed three clusters because of different dominant gut microorganisms which are generated by different habitats. Based on PICRUSt-predicted functions, harmful substance degradation pathways were much more common in cavefish intestinal microorganisms than in those from surface fish. The intestinal microbiota of surface fish group 1 had a higher capacity for carbohydrate metabolism, whereas protein and amino acid metabolism and digestive pathways were more abundant in microorganisms from the cavefish group and surface fish group 2. Combined analysis of the intestinal microbial composition and functional predictions further revealed the structures and functions of intestinal microbial communities in Sinocyclocheilus cave and surface species. Moreover, based on their habits and intestinal microbial composition and intestinal microbial functional predictions, we inferred that the three fish groups were all omnivorous; however, surface fish group 1 preferred feeding on plants, while surface fish group 2 and cavefish preferred meat. This study improves our understanding of mechanisms of adaptation in cave habitats and may contribute to the protection of these habitats from water pollution.
Tài liệu tham khảo
citation_journal_title=Proc Natl Acad Sci U S A; citation_title=Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions; citation_author=AC Aspiras, R Nicolas, M Brian, RL Borowsky, CJ Tabin; citation_volume=112; citation_publication_date=2015; citation_pages=1-6; citation_id=CR1
citation_journal_title=Curr Biol; citation_title=Cavefishes; citation_author=R Borowsky; citation_volume=28; citation_publication_date=2018; citation_pages=60-64; citation_doi=10.1016/j.cub.2017.12.011; citation_id=CR2
citation_journal_title=Mol Biol Evol; citation_title=Evolution of the eye transcriptome under constant darkness in Sinocyclocheilus cavefish; citation_author=F Meng, I Braasch, JB Phillips, X Lin, T Titus, C Zhang, JH Postlethwait; citation_volume=30; citation_publication_date=2013; citation_pages=1527-1543; citation_doi=10.1093/molbev/mst079; citation_id=CR3
citation_journal_title=Journal of Guizhou Normal University (Natural Sciences); citation_title=Elemental study on species diversity of karst cave animals in Shilin area of Yunnan province; citation_author=DH Li, TC Luo; citation_volume=20; citation_publication_date=2002; citation_pages=1-5; citation_id=CR4
citation_title=An introduction to the special volume on the biology of hypogean fishes; citation_inbook_title=The biology of hypogean fishes; citation_publication_date=2001; citation_pages=7-12; citation_id=CR5; citation_author=A Romero; citation_publisher=Springer Netherlands
citation_journal_title=Acta Zootaxon Sin; citation_title=Past research and future development on endemic chinese cavefish of the genus sinocyclocheilus (cypriniformes,cyprinidae); citation_author=YH Zhao; citation_volume=31; citation_publication_date=2006; citation_pages=769-777; citation_id=CR6
citation_journal_title=Aquac Res; citation_title=Role of gastrointestinal microbiota in fish; citation_author=N Sukantak; citation_volume=41; citation_publication_date=2010; citation_pages=1553-1573; citation_id=CR7
citation_journal_title=Aquaculture; citation_title=Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout ( Oncorhynchus mykiss ); citation_author=MJ Pond, DM Stone, DJ Alderman; citation_volume=261; citation_publication_date=2006; citation_pages=194-203; citation_id=CR8
citation_journal_title=Aquaculture; citation_title=Live yeasts in the gut: natural occurrence, dietary introduction, and their effects on fish health and development; citation_author=FJ Gatesoupe; citation_volume=267; citation_publication_date=2007; citation_pages=20-30; citation_id=CR9
citation_journal_title=Acta Zoologica Lituanica; citation_title=Proteolytic Activity of the Roach (Rutilus Rutilus L.) Intestinal Microflora; citation_author=Vesta Skrodenytė-Arbačiauskienė; citation_volume=10; citation_issue=3; citation_publication_date=2000; citation_pages=69-77; citation_id=CR10
citation_journal_title=Fish Sci; citation_title=Assessment of microbial diversity in the river trout Salmo trutta fario L. intestinal tract identified by partial 16S rRNA gene sequence analysis; citation_author=V Skrodenyte-Arbaciauskiene, A Sruoga, D Butkauskas; citation_volume=72; citation_publication_date=2006; citation_pages=597-602; citation_id=CR11
citation_journal_title=FEMS Immunol Med Microbiol; citation_title=A review on the interactions between gut microbiota and innate immunity of fish; citation_author=GD Gómez, JL Balcázar; citation_volume=52; citation_publication_date=2008; citation_pages=145-154; citation_doi=10.1111/j.1574-695X.2007.00343.x; citation_id=CR12
citation_journal_title=Aquaculture; citation_title=Electron microscopy of the intestinal microflora of fish; citation_author=E Ringø, RE Olsen, TM Mayhew, R Myklebust; citation_volume=227; citation_publication_date=2003; citation_pages=395-415; citation_doi=10.1016/j.aquaculture.2003.05.001; citation_id=CR13
citation_journal_title=Biologija; citation_title=Defence mechanisms in fish: frequency of the genus Lactobacillus bacteria in the intestinal tract microflora of carps; citation_author=R Jankauskienë; citation_volume=2; citation_publication_date=2002; citation_pages=13-17; citation_id=CR14
citation_journal_title=Aquac Int; citation_title=Enzyme producing bacterial flora isolated from fish digestive tracts; citation_author=A Bairagi, KS Ghosh, SK Sen, AK Ray; citation_volume=10; citation_publication_date=2002; citation_pages=109-121; citation_id=CR15
citation_journal_title=Dev Biol; citation_title=Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation; citation_author=JM Bates, E Mittge, J Kuhlman, KN Baden, SE Cheesman, K Guillemin; citation_volume=297; citation_publication_date=2006; citation_pages=374-386; citation_id=CR16
citation_journal_title=Aquaculture; citation_title=Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon ( Salmo salar L.); citation_author=MB Hovda, BT Lunestad, R Fontanillas, JT Rosnes; citation_volume=272; citation_publication_date=2007; citation_pages=581-588; citation_id=CR17
citation_journal_title=Aquacultures; citation_title=The development of the gut microbiota in rainbow trout ( Oncorhynchus mykiss ) is affected by first feeding and diet type; citation_author=HC Ingerslev, LVG Jørgensen, ML Strube, N Larsen, I Dalsgaard, M Boye, L Madsen; citation_volume=424–425; citation_publication_date=2014; citation_pages=24-34; citation_id=CR18
citation_journal_title=Aquac Res; citation_title=Characterization of cellulase-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, Ctenopharyngodon idella (Valenciennes); citation_author=S Saha, RN Roy, SK Sen, AK Ray; citation_volume=37; citation_publication_date=2006; citation_pages=380-388; citation_id=CR19
citation_journal_title=Journal of Yunnan Agricultural University; citation_title=Two new species of Sinocycolocheilus form eastern Yunnan, China; citation_author=W Li, Y Liu, H Yang; citation_volume=17; citation_publication_date=2002; citation_pages=58-60; citation_id=CR20
citation_journal_title=Zool Res; citation_title=Four new species of sinocyclocheilus from Yunnan (cypriniformes: cyprinidae: barbinae); citation_author=W Li; citation_volume=6; citation_publication_date=1985; citation_pages=125-129; citation_id=CR21
citation_journal_title=Acta Hydrobiol Sin; citation_title=Description on three species of sinocyclocheilus from Yunnan, China; citation_author=W Li; citation_volume=16; citation_publication_date=1992; citation_pages=57-61; citation_id=CR22
citation_journal_title=Acta Zootaxon Sin; citation_title=A revision of Chinese cyprinid genus sinocyclocheilus with reference to the interspecific relationships; citation_author=XL Chu; citation_volume=10; citation_publication_date=1985; citation_pages=101-107; citation_id=CR23
citation_journal_title=Journal of Zhantiang Fisheries College; citation_title=One new species of sinocyclocheilus from Yunnan; citation_author=W Li, W Mao; citation_volume=22; citation_publication_date=2002; citation_pages=1-3; citation_id=CR24
citation_journal_title=Zool Res; citation_title=Validation and re-description of Sinocyclocheilus aluensis Li et Xiao, 2005 (Cypriniforms: Cyprinidae); citation_author=YH Zhao, CG Zhang; citation_volume=34; citation_publication_date=2013; citation_pages=374-378; citation_id=CR25
citation_journal_title=Journal of Zhantiang Fisheries College; citation_title=A new species of cyprinidae from Yunnan-Sinocyclocheilus rhinocerous; citation_author=W Li; citation_volume=14; citation_publication_date=1994; citation_pages=1-3; citation_id=CR26
citation_journal_title=Zool Syst; citation_title=On a new fish of the genus sinocyclocheilus from Guangxi China (cypriniformes: cyprinidae: barbinae); citation_author=G Li; citation_volume=14; citation_publication_date=1989; citation_pages=126-129; citation_id=CR27
citation_journal_title=Journal of Zhantiang Fisheries College; citation_title=A new genis and three new species of cyprinidae from Guangxi, China; citation_author=W Li, J Lan; citation_volume=12; citation_publication_date=1992; citation_pages=46-51; citation_id=CR28
citation_journal_title=Zoological Systematics; citation_title=One new species of blind cavefish from Guangxi with comments on its phylogenetic status (Cypriniformes:Cyprinidae:Barbinae); citation_author=Y Chen, J Yang, J Lan; citation_volume=22; citation_publication_date=1997; citation_pages=219-223; citation_id=CR29
citation_journal_title=Acta Academiae Medicinae Zunyi; citation_title=A new species of sinocyclocheilus from Guizhou, China (Cypriniformes: Cyprinidae: Barbinae); citation_author=D Wang, J Liao; citation_volume=20; citation_publication_date=1997; citation_pages=1-3; citation_id=CR30
citation_journal_title=Bioinformatics; citation_title=FLASH: fast length adjustment of short reads to improve genome assemblies; citation_author=T Mago, SL Salzberg; citation_volume=27; citation_publication_date=2011; citation_pages=2957-2963; citation_id=CR31
citation_journal_title=Appl Environ Microbiol; citation_title=Altered fecal microbiota composition associated with food allergy in infants; citation_author=Z Ling, Z Li, X Liu, Y Cheng, Y Luo, X Tong, L Yuan, Y Wang, J Sun, L Li; citation_volume=80; citation_publication_date=2014; citation_pages=2546-2554; citation_id=CR32
citation_journal_title=Lett Appl Microbiol; citation_title=Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish; citation_author=C Tsuchiya, T Sakata, H Sugita; citation_volume=46; citation_publication_date=2010; citation_pages=43-48; citation_id=CR33
citation_journal_title=AMB Express; citation_title=Pyrosequencing of 16S rRNA gene amplicons to study the microbiota in the gastrointestinal tract of carp ( Cyprinus carpio L.); citation_author=MAV Kessel, BE Dutilh, K Neveling, MP Kwint, JA Veltman, G Flik, MS Jetten, PH Klaren, HJOD Camp; citation_volume=1; citation_publication_date=2011; citation_pages=41-41; citation_id=CR34
citation_journal_title=Aquaculture; citation_title=Microbial diversity of intestinal contents and mucus in yellow catfish (Pelteobagrus fulvidraco); citation_author=S Wu, T Gao, Y Zheng, W Wang, Y Cheng, G Wang; citation_volume=303; citation_publication_date=2016; citation_pages=1-7; citation_id=CR35
Huang H, Wu X (1987) China economic animal record: freshwater fishes. Science Press
Zhao Y, Zhang C (2009) Endemic fishes of Sinocyclocheilus (Cypriniformes:Cyprinidae) in China. Science press
citation_journal_title=Freshw Fish; citation_title=Biological survey of Sinocyclocheilus maitianheensis; citation_author=WD Li Weixian; citation_volume=29; citation_publication_date=1999; citation_pages=23-24; citation_id=CR38
citation_journal_title=Microb Ecol; citation_title=Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing; citation_author=T Li, M Long, FJ Gatesoupe, Q Zhang, A Li, X Gong; citation_volume=69; citation_publication_date=2015; citation_pages=1-12; citation_id=CR39
citation_journal_title=Journal of Yunnan Agricultural University; citation_title=The preliminary investigation of geographical distribution and ecological adaptation for cave environment of Sinocyclocheilus rhinocerous--a cyprinid fish; citation_author=W Li, D Wu, A Chen, J Tao; citation_volume=15; citation_publication_date=2000; citation_pages=1-4; citation_id=CR40
citation_journal_title=Chin J Oceanol Limnol; citation_title=Comparison of intestinal bacterial communities in grass carp, Ctenopharyngodon idellus, from two different habitats; citation_author=J Ni, Y Yu, T Zhang, L Gao; citation_volume=30; citation_publication_date=2012; citation_pages=757-765; citation_id=CR41
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.
https://doi.org/10.1038/srep24340
citation_journal_title=Br J Nutr; citation_title=Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.); citation_author=AM Bakkemckellep, MH Penn, PM Salas, S Refstie, S Sperstad, T Landsverk, E Ringø, A Krogdahl; citation_volume=97; citation_publication_date=2007; citation_pages=699-713; citation_id=CR43
citation_journal_title=J Appl Microbiol; citation_title=Characterization of the gut microbiota of three commercially valuable warmwater fish species; citation_author=AM Larsen, HH Mohammed, CR Arias; citation_volume=116; citation_publication_date=2014; citation_pages=1396-1404; citation_id=CR44
citation_journal_title=Chin J App Environ Biol; citation_title=Isolation and identification of major cellulase-producing fungi in intestines of grass carp; citation_author=HE Li, B Hao, C Xie, X Luo, Z Zhang, X Zhu; citation_volume=15; citation_publication_date=2009; citation_pages=414-418; citation_id=CR45
citation_journal_title=PLoS One; citation_title=Composition, diversity, and origin of the bacterial community in grass carp intestine; citation_author=S Wu, G Wang, ER Angert, W Wang, W Li, H Zou; citation_volume=7; citation_publication_date=2012; citation_id=CR46
citation_journal_title=Freshwater Fisheries; citation_title=Study on digestive enzyme-producing bacteria from the digestive tract of Ctenopharyngodon idellus and Carassius auratus gibelio; citation_author=X Feng, XW Zhi, DM Zhu, Y Wang, SF Pang, MY Yan, XH Mei, XX Chen; citation_volume=38; citation_publication_date=2008; citation_pages=51-57; citation_id=CR47
citation_journal_title=Journal of Applied Aquaculture; citation_title=Characterization of Bacilli Isolated from the Gut of Rohu,Labeo rohita, Fingerlings and Its Significance in Digestion; citation_author=Koushik Ghosh, Sukanta Kumar Sen, Arun Kumar Ray; citation_volume=12; citation_issue=3; citation_publication_date=2002; citation_pages=33-42; citation_id=CR48
citation_journal_title=Aquac Res; citation_title=Cellulase-producing Bacillus strains isolated from the intestine of Amazon basin fish; citation_author=SB Peixoto, F Cladera-Olivera, DJ Daroit, A Brandelli; citation_volume=42; citation_publication_date=2011; citation_pages=887-891; citation_id=CR49
citation_journal_title=Aquac Nutr; citation_title=Enzyme-producing bacteria isolated from fish gut: a review; citation_author=AK Ray, K Ghosh, E Ringø; citation_volume=18; citation_publication_date=2012; citation_pages=465-492; citation_id=CR50
citation_journal_title=Acta Peadiatrica: Promoting Child Health; citation_title=Establishment of the gut microbiota in Western infants; citation_author=I Adlerberth, AE Wold; citation_volume=98; citation_publication_date=2009; citation_pages=229-238; citation_id=CR51
citation_journal_title=Pharmacological Research; citation_title=Interactions of gut microbiota with functional food components and nutraceuticals; citation_author=J.M. Laparra, Y. Sanz; citation_volume=61; citation_issue=3; citation_publication_date=2010; citation_pages=219-225; citation_id=CR52
citation_journal_title=Carsologica Sinica; citation_title=A survey of speleobiological studies in China; citation_author=J Ran, H Chen; citation_volume=7; citation_publication_date=1998; citation_pages=151-159; citation_id=CR53
citation_journal_title=Sichuan Journal of Zoology; citation_title=Correlation study between cave animal community and the cavern environment in dolomite karst area, Guizhou Province; citation_author=G Zhang, W Yang; citation_volume=34; citation_publication_date=2015; citation_pages=375-382; citation_id=CR54
citation_journal_title=FEMS Microbiol Lett; citation_title=Secreted enzymes of Aeromonas; citation_author=JM Pemberton, SP Kidd, R Schmidt; citation_volume=152; citation_publication_date=1997; citation_pages=1-10; citation_id=CR55
Culver DC, Pipan T (2009) biology of caves and other subterranean habitats. Oxford University Press 38: 309–311
citation_journal_title=PLoS One; citation_title=Discovery of a diverse cave flora in China; citation_author=A Monro, N Bystriakova, L Fu, F Wen, Y Wei; citation_volume=13; citation_publication_date=2018; citation_id=CR57
Claus SP, Guillou H, Ellero-Simatos S (2016) The gut microbiota: a major player in the toxicity of environmental pollutants? NPJ Biofilms & Microbiomes 2:16003.
https://doi.org/10.1038/npjbiofilms.2016.3