野生和室内饲养高原鼠兔肠道菌群多样性的比较
|
摘要
肠道微生物在宿主的生理活动、免疫调节以及健康方面均有重要的作用。尽管已有报道表明高原鼠兔肠道菌群和食物、环境有关,但对于野生和室内饲养条件下,取食不同食物的高原鼠兔肠道菌群是否存在差异尚不清楚。本研究利用16S rRNA基因高通量测序技术比较夏季野生和室内饲养高原鼠兔的肠道菌群发现,与野生鼠兔相比,室内鼠兔有更高丰度的拟杆菌门(Bacteroidetes)和螺旋体门(Spirochetes),更低丰度的变形菌门(Proteobacteria)和放线菌门(Actinobacteria)。野生和室内饲养的鼠兔肠道共有的操作分类单元(operational taxonomic units,OTUs)有50.1%是重叠的,而49.9%的OTUs是各自特有的。野生和室内饲养肠道菌群的组成和群落结构(β多样性)有显著性差异。因此,室内饲养鼠兔不能有效反映野生状态下高原鼠兔肠道菌群的情况。
Gut microbiota play important roles in host physiological activity, immune regulation, and health. Although numerous studies have found that gut microbiota of plateau pikas are related to food and environment, the differences of gut microbiota between wild and laboratory-reared plateau pikas are still unclear. In this study, we used 16 S rRNA gene highthroughput sequencing technology to compare the differences of gut microbial communities between wild and laboratoryreared plateau pikas. Our results suggested that laboratory-reared plateau pikas had higher abundance of Bacteroidetes and Spirochetes, but lower abundance of Proteobacteria and Actinobacteria than wild plateau pikas. There was 50.1% overlap of gut operational taxonomic units(OTUs) between wild and laboratory-reared plateau pikas, while 49.9% of gut OTUs were specific in the wild and laboratory-reared plateau pikas. Significant differences were detected in both composition and community structure(β diversity) of gut microbes in the wild and laboratory-reared plateau pikas. Therefore, laboratoryreared plateau pika could not effectively reflect the gut microbiota of plateau pika in the wild.
Gut microbiota play important roles in host physiological activity, immune regulation, and health. Although numerous studies have found that gut microbiota of plateau pikas are related to food and environment, the differences of gut microbiota between wild and laboratory-reared plateau pikas are still unclear. In this study, we used 16 S rRNA gene highthroughput sequencing technology to compare the differences of gut microbial communities between wild and laboratoryreared plateau pikas. Our results suggested that laboratory-reared plateau pikas had higher abundance of Bacteroidetes and Spirochetes, but lower abundance of Proteobacteria and Actinobacteria than wild plateau pikas. There was 50.1% overlap of gut operational taxonomic units(OTUs) between wild and laboratory-reared plateau pikas, while 49.9% of gut OTUs were specific in the wild and laboratory-reared plateau pikas. Significant differences were detected in both composition and community structure(β diversity) of gut microbes in the wild and laboratory-reared plateau pikas. Therefore, laboratoryreared plateau pika could not effectively reflect the gut microbiota of plateau pika in the wild.
引文
[1]TREMAROLI V,BACKHED F.Functional interactions between the gut microbiota and host metabolism.Nature,2012,489:242-249.
[2]ZHANG H,SPARKS J B,KARYALA S V,SETTLAGE R,LUO X M.Host adaptive immunity alters gut microbiota.The ISMEJournal,2015,9(3):770-781.
[3]GAGNIERE J,RAISCH J,VEZIANT J,BARNICH N,BONNET R,BUC E,BRINGER M A,PEZET D,BONNET M.Gut microbiota imbalance and colorectal cancer.World Journal of Gastroenterology,2016,22(2):501-518.
[4]丁赟,吴琦,胡义波,王潇,聂永刚,吴小平,魏辅文.野生哺乳动物肠道微生物组研究进展与展望.兽类学报,2017,37(4):399-406.DING Y,WU Q,HU Y B,WANG X,NIE Y G,WU X P,WEI F W.Advances and prospects of gut microbiome in wild mammals.Acta Theriologica Sinica,2017,37(4):399-406.
[5]TURNBAUGH P J,BACKHED F,FULTON L,GORDON J I.Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome.Cell Host&Microbe,2008,3(4):213-223.
[6]MUEGGE B D,KUCZYNSKI J,KNIGHTS D,CLEMENTE J C,GONZALEZ A,FONTANA L,HENRISSAT B,KNIGHT R,GORDON J I.Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans.Science,2011,332(6032):970-974.
[7]CARMODY R N,GERBER G K,LUEVANO J M,GATTI D M,SOMES L,SVENSON K L,TURNBAUGH P J.Diet dominates host genotype in shaping the murine gut microbiota.Cell Host&Microbe,2015,17(1):72-84.
[8]PEREZ-COBAS A E,MAIQUES E,ANGELOVA A,CARRASCO P,MOYA A,LATORRE A.Diet shapes the gut microbiota of the omnivorous cockroach Blattella germanica.FEMS Microbiology Ecology,2015,91(4):1-14.
[9]MONTLLOR C B,MAXMEN A,PURCELL A H.Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress.Ecological Entomology,2002,27(2):189-195.
[10]TSUCHIDA T,KOGA R,FUKATSU T.Host plant specialization governed by facultative symbiont.Science,2004,303:1989-1989.
[11]KOHL K D,VARNER J,WILKENING J L,DEARING M D.Gut microbial communities of American pikas(Ochotona princeps):Evidence for phylosymbiosis and adaptations to novel diets.Journal of Animal Ecology,2017,87(2):323-330.
[12]NAYAK S K.Probiotics and immunity:A fish perspective.Fish&Shellfish Immunology,2010,29(1):2-14.
[13]WANG G X,LIU Y T,LI F Y,GAO H T,LEI Y,LIU X L.Immunostimulatory activities of Bacillus simplex DR-834 to carp(Cyprinus carpio).Fish&Shellfish Immunology,2010,29(3):378-387.
[14]LIU C H,CHIU C H,WANG S W,CHENG W.Dietary administration of the probiotic,Bacillus subtilis E20,enhances the growth,innate immune responses,and disease resistance of the grouper,Epinephelus coioides.Fish&Shellfish Immunology,2012,33(4):699-706.
[15]HAO K,WU Z Q,LI D L,YU X B,WANG G X,LING F.Effects of dietary administration of Shewanella xiamenensis A-1,Aeromonas veronii A-7,and Bacillus subtilis,single or combined,on the grass carp(Ctenopharyngodon Idella)intestinal microbiota.Probiotics and Antimicrobial Proteins,2017,9(4):386-396.
[16]VISPO C,KARASOV W H.The interactions of avian gut microbes and their host:An elusive symbiosis.Gastrointestinal Microbiology,1997:116-155.
[17]WIENEMANN T,SCHMITT-WAGNER D,MEUSER K,SEGELBACHER G,SCHINK B,BRUNE A,BERTHOLD P.The bacterial microbiota in the ceca of Capercaillie(Tetrao urogallus)differs between wild and captive birds.Systematic and Applied Microbiology,2011,34(7):542-551.
[18]QIN J,LI R,RAES J,ARUMUGAM M,BURGDORF K S,MANICHANH C,NIELSEN T,PONS N,LEVENEZ F,YAMADA T,MENDE D R,LI J,XU J,LI S,LI D,CAO J,WANG B,LIANG H,ZHENG H,XIE Y,TAP J,LEPAGE P,BERTALAN M,BATTO J M,HANSEN T,PASLIER D L,LINNEBERG A,NIELSEN H B,PELLETIER E,RENAULT P,SICHERITZ-PONTENT,TURNER K,ZHU H,YU C,LI S,JIAN M,ZHOU Y,LI Y,ZHANG X,LI S,QIN N,YANG H,WANG J,BRUNAK S,DOREJ,GUARNER F,KRISTIANSEN K,PEDERSEN O,PARKHILL J,WEISSENBACH J,CONSORTIUM M,BORK P,EHRLICHS D,WANG J.A human gut microbial gene catalogue established by metagenomic sequencing.Nature,2010,464:59-65.
[19]VIJAY-KUMAR M,AITKEN J D,CARVALHO F A,CULLENDER T C,MWANGI S,SRINIVASAN S,SITARAMAN S V,KNIGHT R,LEY R E,GEWIRTZ A T.Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5.Science,2010,328:228-231.
[20]DIAZ HEIJTZ R,WANG S,ANUAR F,QIAN Y,BJORKHOLM B,SAMUELSSON A,HIBBERD M L,FORSSBERG H,PETTERSSON S.Normal gut microbiota modulates brain development and behavior.Proceedings of the National Academy of Sciences of the United States of America,2011,108(7):3047-3052.
[21]LI L,ZHAO X.Comparative analyses of fecal microbiota in Tibetan and Chinese Han living at low or high altitude by barcoded454 pyrosequencing.Scientific Reports,2015,5:14682.
[22]TANG W,XING Z,HU W,LI C,WANG J,WANG Y.Antioxidative effects in vivo and colonization of Lactobacillus plantarum MA2 in the murine intestinal tract.Applied Microbiology and Biotechnology,2016,100(16):7193-7202.
[23]SMITH A T,XIE Y.A Guide to the Mammals of China.Princeton:Princeton University Press,2008.
[24]蒋志刚,夏武平.高原鼠兔食物资源利用的研究.兽类学报,1985,5(4):251-262.JIANG Z G,XIA W P.Utilization of the food resources by plateau pika.Acta Theriologica Sinica,1985,5(4):251-262.
[25]王溪,刘季科,刘伟,纪兰菊.植食性小哺乳类营养生态学的研究:高原鼠兔的食物选择模式与食物质量.兽类学报,1992,12(3):183-192.WANG X,LIU J K,LIU W,JI L J.Studies on the nutritional ecology reseach of herbivorous small mammals:Patterns of food selection and food quality for plateau pika,Ochotona curzoniae.Acta Theriologica Sinica,1992,12(3):183-192.
[26]SMITH A T,FOGGIN J M.The plateau pika(Ochotona curzoniae)is a keystone species for biodiversity on the Tibetan plateau.Animal Conservation,1999,2(4):235-240.
[27]SMITH A T,LAI C H.Keystone status of plateau pikas(Ochotona curzoniae):Effect of control on biodiversity of native birds.Biodiversity and Conservation,2003,12(9):1901-1912.
[28]LI H,LI T,BEASLEY D E,HEDENEC P,XIAO Z,ZHANG S,LI J,LIN Q,LI X.Diet diversity is associated with beta but not alpha diversity of pika gut microbiota.Frontiers in Microbiology,2016,7:1169.
[29]LI H,QU J,LI T,LI J,LIN Q,LI X.Pika population density is associated with the composition and diversity of gut microbiota.Frontiers in Microbiology,2016c,7:758.
[30]LI H,LI T,YAO M,LI J,ZHANG S,WIRTH S,CAO W,LIN Q,LI X.Pika gut may select for rare but diverse environmental bacteria.Frontiers in Microbiology,2016b,7:1269.
[31]KOHL K D,DEARING M D.Experience matters:prior exposure to plant toxins enhances diversity of gut microbes in herbivores.Ecology Letters,2012,15(9):1008-1015.
[32]VILLERS L M,JANG S S,LENT C L,LEWIN-KOH S C,NOROSOARINALVO J A.Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur(Lemur catta)populations.American Journal of Primatology:Official Journal of the American Society of Primatologists,2008,70(2):175-184.
[33]NADEEM O K,NIDHI S,JEREMY W C,JULIAN MC,STEPLEN M R,HAZEL M M.The interplay between campylobacter and helicobacter species and other gastrointestinal microbiota of commercial broiler chickens.Systematic and Applied Microbiology,2016(6):18.
[34]TAMAKI H,WRIGHT C L,LI X,LIN Q,HWANG C,WANG S,THIMMAPURAM J,KAMAGATA Y,LIU W.Analysis of 16SrRNA amplicon sequencing options on the roche/454 next-generation titanium sequencing platform.PLoS ONE,2011,6(9):e25263.
[35]CAPORASO J G,LAUBER C L,WALTERS W A,BERG-LYONS D,HUNTLEY J,FIERER N,OWENS S M,BETLEY J,FRASER L,BAUER M,GORMLEY N,GILBERT J A,SMITH G,KNIGHT R.Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.The ISME Journal,2012,6(8):1621-1624.
[36]MAGOC T,SALZBERG S L.FLASH:fast length adjustment of short reads to improve genome assemblies.Bioinformatics,2011,27(21):2957-2963.
[37]BENGTSSON-PALME J,HARTMANN M,ERIKSSON K M,PAL C,THORELL K,LARSSON D G,NILSSON R H.Metaxa2:Improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data.Molecular Ecology Resources,2015,15(6):1403-1414.
[38]EDGAR R C,HAAS B J,CLEMENTE J C,QUINCE C,KNIGHT R.Uchime improves sensitivity and speed of chimera detection.Bioinformatics,2011,27(16):2194-2200.
[39]LI W,GODZIK A.CD-HIT:A fast program for clustering and comparing large sets of protein or nucleotide sequences.Bioinformatics,2006,22(13):1658-1659.
[40]LOZUPONE C,KNIGHT R.UniFrac:A new phylogenetic method for comparing microbial communities.Applied and Environmental Microbiology,2005,71(12):8228-8235.
[41]ORMEROD K L,WOOD D L A,LACHNER N,GELLATLY S L,DALY J N,PARSONS J D,DALMOLIN C G O,PALFREYMAN R W,NIELSEN L K,COOPER M A,MORRISON M,HANSBRO P M,HUGENHOLTZ P.Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals.Microbiome,2016,4(1):36.
[42]ANDERSON I,ABT B,LYKIDIS A,KLENK H P,KYRPIDES N,IVANOVA N.Genomics of aerobic cellulose utilization systems in actinobacteria.PLoS One,2012,7(6):e39331.
[43]WAKABAYASHI H,OTOTAKE M.Characteristics of extracellular products of Flavobacterium sp.,a pathogen of bacterial gill disease.Fish Pathology,1985,20(2/3):167-171.
[44]VANCANNEYT M,SEGERS P,HAUBEN L,HOMMEZ J,DEVRIESE L A,HOSTE B,VANDAMME P,KERSTERS K.Flavobacterium meningosepticum,a pathogen in birds.Journal of Clinical Microbiology,1994,32(10):2398-2403.
[45]KUNERT A,LOSSE J,GRUSZIN C,HUHN M,KAENDLER K,MIKKAT S,VOLKE D,HOFFMANN R,JOKIRANTA T S,SEEBERGER H,MOELLMANN U,HELLWAGE J,ZIPFEL P F.Immune evasion of the human pathogen pseudomonas aeruginosa:Elongation factor tuf is a factor h and plasminogen binding protein.European Journal of Immunology,2007,179(5):2979-2988.
[46]QU J,LI W,YANG M,JI W,ZHANG Y.Life history of the plateau pika(Ochotona curzoniae)in alpine meadows of the Tibetan Plateau.Mammalian Biology,2013,78(1):68-72.
[47]QU J,RUSSELL J C,JI W,YANG M,CHEN Q,LI W,ZHANG Y.Five-year population dynamics of plateau pikas(Ochotona curzoniae)on the east of Tibetan Plateau.European Journal of Wildlife Research,2017,63(3):51.
[48]SCUPHAM A J,PATTON T G,BENT E,BAYLES D O.Comparison of the cecal microbiota of domestic and wild turkeys.Microbial Ecology,2008,56(2):322-331.
[49]NELSON T M,ROGERS T L,CARLINI A R,BROWN M V.Diet and phylogeny shape the gut microbiota of Antartic seals:Acomparison of wild and captive animals.Environmental Microbiology,2013,15(4):1132-1145.
[50]GHOUL M,MITRI S.The ecology and evolution of microbial competition.Trends in Microbiology,2016,24(10):833-845.
[51]LEY R E,HAMADY M,LOZUPONE C,TURNBAUGH P J,RAMEY R R,BIRCHER J S.Evolution of mammals and their gut microbes.Science,2008,320(5883):1647-1651.
[52]AMATO K R,YEOMAN C J,KENT A,RIGHINI N,CARBONERO F,ESTRADA A,GASKINS H R,STUMPF R M,YILDIRIM S,TORRALBA M,WILSON B A,NELSON K E,WHITE B A,LEIGH S R,GILLIS M.Habitat degradation impacts black howler monkey(Alouatta pigra)gastrointestinal microbiomes.The ISME Journal,2013,7(7):1344-1353.
[2]ZHANG H,SPARKS J B,KARYALA S V,SETTLAGE R,LUO X M.Host adaptive immunity alters gut microbiota.The ISMEJournal,2015,9(3):770-781.
[3]GAGNIERE J,RAISCH J,VEZIANT J,BARNICH N,BONNET R,BUC E,BRINGER M A,PEZET D,BONNET M.Gut microbiota imbalance and colorectal cancer.World Journal of Gastroenterology,2016,22(2):501-518.
[4]丁赟,吴琦,胡义波,王潇,聂永刚,吴小平,魏辅文.野生哺乳动物肠道微生物组研究进展与展望.兽类学报,2017,37(4):399-406.DING Y,WU Q,HU Y B,WANG X,NIE Y G,WU X P,WEI F W.Advances and prospects of gut microbiome in wild mammals.Acta Theriologica Sinica,2017,37(4):399-406.
[5]TURNBAUGH P J,BACKHED F,FULTON L,GORDON J I.Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome.Cell Host&Microbe,2008,3(4):213-223.
[6]MUEGGE B D,KUCZYNSKI J,KNIGHTS D,CLEMENTE J C,GONZALEZ A,FONTANA L,HENRISSAT B,KNIGHT R,GORDON J I.Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans.Science,2011,332(6032):970-974.
[7]CARMODY R N,GERBER G K,LUEVANO J M,GATTI D M,SOMES L,SVENSON K L,TURNBAUGH P J.Diet dominates host genotype in shaping the murine gut microbiota.Cell Host&Microbe,2015,17(1):72-84.
[8]PEREZ-COBAS A E,MAIQUES E,ANGELOVA A,CARRASCO P,MOYA A,LATORRE A.Diet shapes the gut microbiota of the omnivorous cockroach Blattella germanica.FEMS Microbiology Ecology,2015,91(4):1-14.
[9]MONTLLOR C B,MAXMEN A,PURCELL A H.Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress.Ecological Entomology,2002,27(2):189-195.
[10]TSUCHIDA T,KOGA R,FUKATSU T.Host plant specialization governed by facultative symbiont.Science,2004,303:1989-1989.
[11]KOHL K D,VARNER J,WILKENING J L,DEARING M D.Gut microbial communities of American pikas(Ochotona princeps):Evidence for phylosymbiosis and adaptations to novel diets.Journal of Animal Ecology,2017,87(2):323-330.
[12]NAYAK S K.Probiotics and immunity:A fish perspective.Fish&Shellfish Immunology,2010,29(1):2-14.
[13]WANG G X,LIU Y T,LI F Y,GAO H T,LEI Y,LIU X L.Immunostimulatory activities of Bacillus simplex DR-834 to carp(Cyprinus carpio).Fish&Shellfish Immunology,2010,29(3):378-387.
[14]LIU C H,CHIU C H,WANG S W,CHENG W.Dietary administration of the probiotic,Bacillus subtilis E20,enhances the growth,innate immune responses,and disease resistance of the grouper,Epinephelus coioides.Fish&Shellfish Immunology,2012,33(4):699-706.
[15]HAO K,WU Z Q,LI D L,YU X B,WANG G X,LING F.Effects of dietary administration of Shewanella xiamenensis A-1,Aeromonas veronii A-7,and Bacillus subtilis,single or combined,on the grass carp(Ctenopharyngodon Idella)intestinal microbiota.Probiotics and Antimicrobial Proteins,2017,9(4):386-396.
[16]VISPO C,KARASOV W H.The interactions of avian gut microbes and their host:An elusive symbiosis.Gastrointestinal Microbiology,1997:116-155.
[17]WIENEMANN T,SCHMITT-WAGNER D,MEUSER K,SEGELBACHER G,SCHINK B,BRUNE A,BERTHOLD P.The bacterial microbiota in the ceca of Capercaillie(Tetrao urogallus)differs between wild and captive birds.Systematic and Applied Microbiology,2011,34(7):542-551.
[18]QIN J,LI R,RAES J,ARUMUGAM M,BURGDORF K S,MANICHANH C,NIELSEN T,PONS N,LEVENEZ F,YAMADA T,MENDE D R,LI J,XU J,LI S,LI D,CAO J,WANG B,LIANG H,ZHENG H,XIE Y,TAP J,LEPAGE P,BERTALAN M,BATTO J M,HANSEN T,PASLIER D L,LINNEBERG A,NIELSEN H B,PELLETIER E,RENAULT P,SICHERITZ-PONTENT,TURNER K,ZHU H,YU C,LI S,JIAN M,ZHOU Y,LI Y,ZHANG X,LI S,QIN N,YANG H,WANG J,BRUNAK S,DOREJ,GUARNER F,KRISTIANSEN K,PEDERSEN O,PARKHILL J,WEISSENBACH J,CONSORTIUM M,BORK P,EHRLICHS D,WANG J.A human gut microbial gene catalogue established by metagenomic sequencing.Nature,2010,464:59-65.
[19]VIJAY-KUMAR M,AITKEN J D,CARVALHO F A,CULLENDER T C,MWANGI S,SRINIVASAN S,SITARAMAN S V,KNIGHT R,LEY R E,GEWIRTZ A T.Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5.Science,2010,328:228-231.
[20]DIAZ HEIJTZ R,WANG S,ANUAR F,QIAN Y,BJORKHOLM B,SAMUELSSON A,HIBBERD M L,FORSSBERG H,PETTERSSON S.Normal gut microbiota modulates brain development and behavior.Proceedings of the National Academy of Sciences of the United States of America,2011,108(7):3047-3052.
[21]LI L,ZHAO X.Comparative analyses of fecal microbiota in Tibetan and Chinese Han living at low or high altitude by barcoded454 pyrosequencing.Scientific Reports,2015,5:14682.
[22]TANG W,XING Z,HU W,LI C,WANG J,WANG Y.Antioxidative effects in vivo and colonization of Lactobacillus plantarum MA2 in the murine intestinal tract.Applied Microbiology and Biotechnology,2016,100(16):7193-7202.
[23]SMITH A T,XIE Y.A Guide to the Mammals of China.Princeton:Princeton University Press,2008.
[24]蒋志刚,夏武平.高原鼠兔食物资源利用的研究.兽类学报,1985,5(4):251-262.JIANG Z G,XIA W P.Utilization of the food resources by plateau pika.Acta Theriologica Sinica,1985,5(4):251-262.
[25]王溪,刘季科,刘伟,纪兰菊.植食性小哺乳类营养生态学的研究:高原鼠兔的食物选择模式与食物质量.兽类学报,1992,12(3):183-192.WANG X,LIU J K,LIU W,JI L J.Studies on the nutritional ecology reseach of herbivorous small mammals:Patterns of food selection and food quality for plateau pika,Ochotona curzoniae.Acta Theriologica Sinica,1992,12(3):183-192.
[26]SMITH A T,FOGGIN J M.The plateau pika(Ochotona curzoniae)is a keystone species for biodiversity on the Tibetan plateau.Animal Conservation,1999,2(4):235-240.
[27]SMITH A T,LAI C H.Keystone status of plateau pikas(Ochotona curzoniae):Effect of control on biodiversity of native birds.Biodiversity and Conservation,2003,12(9):1901-1912.
[28]LI H,LI T,BEASLEY D E,HEDENEC P,XIAO Z,ZHANG S,LI J,LIN Q,LI X.Diet diversity is associated with beta but not alpha diversity of pika gut microbiota.Frontiers in Microbiology,2016,7:1169.
[29]LI H,QU J,LI T,LI J,LIN Q,LI X.Pika population density is associated with the composition and diversity of gut microbiota.Frontiers in Microbiology,2016c,7:758.
[30]LI H,LI T,YAO M,LI J,ZHANG S,WIRTH S,CAO W,LIN Q,LI X.Pika gut may select for rare but diverse environmental bacteria.Frontiers in Microbiology,2016b,7:1269.
[31]KOHL K D,DEARING M D.Experience matters:prior exposure to plant toxins enhances diversity of gut microbes in herbivores.Ecology Letters,2012,15(9):1008-1015.
[32]VILLERS L M,JANG S S,LENT C L,LEWIN-KOH S C,NOROSOARINALVO J A.Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur(Lemur catta)populations.American Journal of Primatology:Official Journal of the American Society of Primatologists,2008,70(2):175-184.
[33]NADEEM O K,NIDHI S,JEREMY W C,JULIAN MC,STEPLEN M R,HAZEL M M.The interplay between campylobacter and helicobacter species and other gastrointestinal microbiota of commercial broiler chickens.Systematic and Applied Microbiology,2016(6):18.
[34]TAMAKI H,WRIGHT C L,LI X,LIN Q,HWANG C,WANG S,THIMMAPURAM J,KAMAGATA Y,LIU W.Analysis of 16SrRNA amplicon sequencing options on the roche/454 next-generation titanium sequencing platform.PLoS ONE,2011,6(9):e25263.
[35]CAPORASO J G,LAUBER C L,WALTERS W A,BERG-LYONS D,HUNTLEY J,FIERER N,OWENS S M,BETLEY J,FRASER L,BAUER M,GORMLEY N,GILBERT J A,SMITH G,KNIGHT R.Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.The ISME Journal,2012,6(8):1621-1624.
[36]MAGOC T,SALZBERG S L.FLASH:fast length adjustment of short reads to improve genome assemblies.Bioinformatics,2011,27(21):2957-2963.
[37]BENGTSSON-PALME J,HARTMANN M,ERIKSSON K M,PAL C,THORELL K,LARSSON D G,NILSSON R H.Metaxa2:Improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data.Molecular Ecology Resources,2015,15(6):1403-1414.
[38]EDGAR R C,HAAS B J,CLEMENTE J C,QUINCE C,KNIGHT R.Uchime improves sensitivity and speed of chimera detection.Bioinformatics,2011,27(16):2194-2200.
[39]LI W,GODZIK A.CD-HIT:A fast program for clustering and comparing large sets of protein or nucleotide sequences.Bioinformatics,2006,22(13):1658-1659.
[40]LOZUPONE C,KNIGHT R.UniFrac:A new phylogenetic method for comparing microbial communities.Applied and Environmental Microbiology,2005,71(12):8228-8235.
[41]ORMEROD K L,WOOD D L A,LACHNER N,GELLATLY S L,DALY J N,PARSONS J D,DALMOLIN C G O,PALFREYMAN R W,NIELSEN L K,COOPER M A,MORRISON M,HANSBRO P M,HUGENHOLTZ P.Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals.Microbiome,2016,4(1):36.
[42]ANDERSON I,ABT B,LYKIDIS A,KLENK H P,KYRPIDES N,IVANOVA N.Genomics of aerobic cellulose utilization systems in actinobacteria.PLoS One,2012,7(6):e39331.
[43]WAKABAYASHI H,OTOTAKE M.Characteristics of extracellular products of Flavobacterium sp.,a pathogen of bacterial gill disease.Fish Pathology,1985,20(2/3):167-171.
[44]VANCANNEYT M,SEGERS P,HAUBEN L,HOMMEZ J,DEVRIESE L A,HOSTE B,VANDAMME P,KERSTERS K.Flavobacterium meningosepticum,a pathogen in birds.Journal of Clinical Microbiology,1994,32(10):2398-2403.
[45]KUNERT A,LOSSE J,GRUSZIN C,HUHN M,KAENDLER K,MIKKAT S,VOLKE D,HOFFMANN R,JOKIRANTA T S,SEEBERGER H,MOELLMANN U,HELLWAGE J,ZIPFEL P F.Immune evasion of the human pathogen pseudomonas aeruginosa:Elongation factor tuf is a factor h and plasminogen binding protein.European Journal of Immunology,2007,179(5):2979-2988.
[46]QU J,LI W,YANG M,JI W,ZHANG Y.Life history of the plateau pika(Ochotona curzoniae)in alpine meadows of the Tibetan Plateau.Mammalian Biology,2013,78(1):68-72.
[47]QU J,RUSSELL J C,JI W,YANG M,CHEN Q,LI W,ZHANG Y.Five-year population dynamics of plateau pikas(Ochotona curzoniae)on the east of Tibetan Plateau.European Journal of Wildlife Research,2017,63(3):51.
[48]SCUPHAM A J,PATTON T G,BENT E,BAYLES D O.Comparison of the cecal microbiota of domestic and wild turkeys.Microbial Ecology,2008,56(2):322-331.
[49]NELSON T M,ROGERS T L,CARLINI A R,BROWN M V.Diet and phylogeny shape the gut microbiota of Antartic seals:Acomparison of wild and captive animals.Environmental Microbiology,2013,15(4):1132-1145.
[50]GHOUL M,MITRI S.The ecology and evolution of microbial competition.Trends in Microbiology,2016,24(10):833-845.
[51]LEY R E,HAMADY M,LOZUPONE C,TURNBAUGH P J,RAMEY R R,BIRCHER J S.Evolution of mammals and their gut microbes.Science,2008,320(5883):1647-1651.
[52]AMATO K R,YEOMAN C J,KENT A,RIGHINI N,CARBONERO F,ESTRADA A,GASKINS H R,STUMPF R M,YILDIRIM S,TORRALBA M,WILSON B A,NELSON K E,WHITE B A,LEIGH S R,GILLIS M.Habitat degradation impacts black howler monkey(Alouatta pigra)gastrointestinal microbiomes.The ISME Journal,2013,7(7):1344-1353.