Metagenomic comparison of the rectal microbiota between rhesus macaques(Macaca mulatta) and cynomolgus macaques(Macaca fascicularis)
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摘要
Rhesus macaques(Macaca mulatta) and cynomolgus macaques(Macaca fascicularis) are frequently used in establishing animal models for human diseases. To determine the differences in gut microbiota between these species, rectal swabs from 20 rhesus macaques and 21 cynomolgus macaques were collected, and the microbial composition was examined by deep sequencing of the 16 S rR NA gene. We found that the rectal microbiota of cynomolgus macaques exhibited significantly higher alpha diversity than that of rhesus macaques, although the observed number of operational taxonomic units(OTUs) was almost the same. The dominant taxa at both the phylum and genus levels were similar between the two species, although the relative abundances of these dominant taxa were significantly different between them. Phylogenetic Investigation of Communities by Reconstruction of Unobserved States(PICRUSt) showed significant differences in the functional components between the microbiota of the two species, in particular the lipopolysaccharide(LPS) synthesis proteins. The above data indicated significant differences in microbial composition and function between these two closely related macaque species, which should be taken into consideration in the future selection of these animals for disease models.
Rhesus macaques(Macaca mulatta) and cynomolgus macaques(Macaca fascicularis) are frequently used in establishing animal models for human diseases. To determine the differences in gut microbiota between these species, rectal swabs from 20 rhesus macaques and 21 cynomolgus macaques were collected, and the microbial composition was examined by deep sequencing of the 16 S rR NA gene. We found that the rectal microbiota of cynomolgus macaques exhibited significantly higher alpha diversity than that of rhesus macaques, although the observed number of operational taxonomic units(OTUs) was almost the same. The dominant taxa at both the phylum and genus levels were similar between the two species, although the relative abundances of these dominant taxa were significantly different between them. Phylogenetic Investigation of Communities by Reconstruction of Unobserved States(PICRUSt) showed significant differences in the functional components between the microbiota of the two species, in particular the lipopolysaccharide(LPS) synthesis proteins. The above data indicated significant differences in microbial composition and function between these two closely related macaque species, which should be taken into consideration in the future selection of these animals for disease models.
Rhesus macaques(Macaca mulatta) and cynomolgus macaques(Macaca fascicularis) are frequently used in establishing animal models for human diseases. To determine the differences in gut microbiota between these species, rectal swabs from 20 rhesus macaques and 21 cynomolgus macaques were collected, and the microbial composition was examined by deep sequencing of the 16 S rR NA gene. We found that the rectal microbiota of cynomolgus macaques exhibited significantly higher alpha diversity than that of rhesus macaques, although the observed number of operational taxonomic units(OTUs) was almost the same. The dominant taxa at both the phylum and genus levels were similar between the two species, although the relative abundances of these dominant taxa were significantly different between them. Phylogenetic Investigation of Communities by Reconstruction of Unobserved States(PICRUSt) showed significant differences in the functional components between the microbiota of the two species, in particular the lipopolysaccharide(LPS) synthesis proteins. The above data indicated significant differences in microbial composition and function between these two closely related macaque species, which should be taken into consideration in the future selection of these animals for disease models.
引文
Bhanedd F,Ley RE,Sonnenburg JL,Peterson DA,Gordon JI.2005.Host-bacterial mutualism in the human intestine.Science,307(5717):1915-1920.
Bauer SA,Arndt TP,Leslie KE,Pearl DL,Turner PY.2011.Obesity in rhesus and cynomolgus macaques:a comparative review of the condition and its implications for research.Comparative Medicine,61(6):514-526.
Bernard NJ.2014.Rheumatoid arthritis:Prevotella copri associated with new-onset untreated RA.Nature Reviews Rheumatology,10(1):2.
Dillon SM,Lee EJ,Kotter CV,Austin GL,Gianella S,Siewe B,Smith DM,Landay AL,Mcmanus MC,Robertson CE,Frank DN,Mccarter MD,Wilson CC.2016.Gut dendritic cell activation links an altered colonic microbiome to mucosal and systemic T-cell activation in untreated HIV-1 infection.Mucosal Immunology,9(1):24-37.
Euler AR,Zurenko GE,Moe JB,Ulrich RG,Yagi Y.1990.Evaluation of two monkey species(Macaca mulatta and Macaca fascicularis)as possible models for human Helicobacter pylori disease.Journal of Clinical Microbiology,28(10):2285-2290.
Feichtinger H,Putkonen P,Parravicini C,Li SL,Kaaya EE,Bottiger D,Biberfeld G,Biberfeld P.1990.Malignant lymphomas in cynomolgus monkeys infected with simian immunodeficiency virus.American Journal of Pathology,137(6):1311-1315.
Kaiko GE,Stappenbeck TS.2014.Host-microbe interactions shaping the gastrointestinal environment.Trends in Immunology,35(11):538-548.
Klatt NR,Harris LD,Vinton CL,Sung H,Briant JA,Tabb B,Morcock D,Mcginty JW,Lifson JD,Lafont BA,Martin MA,Levine AD,Estes JD,Brenchley JM.2010.Compromised gastrointestinal integrity in pigtail macaques is associated with increased microbial translocation,immune activation,and IL-17 production in the absence of SIV infection.Mucosal Immunology,3(4):387-398.
Langille MG,Zaneveld J,Caporaso JG,Mcdonald D,Knights D,Reyes JA,Clemente JC,Burkepile DE,Vega Thurber RL,Knight R,Beiko RG,Huttenhower C.2013.Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences.Nature Biotechnology,31(9):814-821.
Lathrop SK,Bloom SM,Rao SM,Nutsch K,Lio CW,Santacruz N,Peterson DA,Stappenbeck TS,Hsieh CS.2011.Peripheral education of the immune system by colonic commensal microbiota.Nature,478(7368):250-254.
Letvin NL,Daniel MD,Sehgal PK,Desrosiers RC,Hunt RD,Waldron LM,Mackey JJ,Schmidt DK,Chalifoux LV,King NW.1985.Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III.Science,230(4721):71-73.
Li D,Wang FJ,Yu L,Yao WR,Cui YF,Yang GB.2017.Expression of pIgRin the tracheal mucosa of SHIV/SIV-infected rhesus macaques.Zoological Research,38(1):44-48.
Loftin KC,Brown LR,Levy BM.1980.Comparison of the predominant cultivable microflora in the dental plaque of Macaca mulatta(rhesus)and Macaca fascicularis(cynomolgus).Journal of Dental Research,59(10):1606-1612.
Lozupone C,Lladser ME,Knights D,Stombaugh J,Knight R.2011.UniFrac:an effective distance metric for microbial community comparison.The ISMEJournal,5(2):169-172.
Manichanh C,Rigottier-Gois L,Bonnaud E,Gloux K,Pelletier E,Frangeul L,Nalin R,Jarrin C,Chardon P,Marteau P,Roca J,Dore J.2006.Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach.Gut,55(2):205-211.
Niess JH,Adler G.2010.Enteric flora expands gut lamina propria CX3CR1+dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions.Journal of Immunology,184(4):2026-2037.
Parks DH,Tyson GW,Hugenholtz P,Beiko RG.2014.STAMP:statistical analysis of taxonomic and functional profiles.Bioinformatics,30(21):3123-3124.
Rawls JF,Mahowald MA,Ley RE,Gordon JI.2006.Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection.Cell,127(2):423-433.
Reimann KA,Parker RA,Seaman MS,Beaudry K,Beddall M,Peterson L,Williams KE,Veazey RS,Montefiori DC,Mascola JR,Nabel GJ,Letvin NL.2005.Pathogenicity of simian-human immunodeficiency virus SHIV-89.6Pand SIVmac is attenuated in cynomolgus macaques and associated with early T-lymphocyte responses.Journal of Virology,79(14):8878-8885.
Rieder R,Wisniewski PJ,Alderman BL,Campbell SC.2017.Microbes and mental health:A review.Brain,Behavior,and Immunity,66:9-17.
Sokol H,Pigneur B,Watterlot L,Lakhdari O,Bermudez-Humaran LG,Gratadoux JJ,Blugeon S,Bridonneau C,Furet JP,Corthier G,Grangette C,Vasquez N,Pochart P,Trugnan G,Thomas G,Blottiere HM,Dore J,Marteau P,Seksik P,Langella P.2008.Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients.Proceedings of the National Academy of Sciences of the United States of America,105(43):16731-16736.
Stilling RM,Ryan FJ,Hoban AE,Shanahan F,Clarke G,Claesson MJ,Dinan TG,Cryan JF.2015.Microbes&neurodevelopment-Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala.Brain,Behavior,and Immunity,50:209-220.
ten Haaft P,Almond N,Biberfeld G,Cafaro A,Cranage M,Ensoli B,Hunsmann G,Polyanskaya N,Stahl-Hennig C,Thortensson R,Titti F,Heeney J.2001.Comparison of early plasma RNA loads in different macaque species and the impact of different routes of exposure on SIV/SHIVinfection.Journal of Medical Primatology,30(4):207-214.
Tilg H,Moschen AR.2014.Microbiota and diabetes:an evolving relationship.Gut,63(9):1513-1521.
van Nood E,Vrieze A,Nieuwdorp M,Fuentes S,Zoetendal EG,de Vos WM,Visser CE,Kuijper EJ,Bartelsman JF,Tijssen JG,Speelman P,Dijkgraaf MG,Keller JJ.2013.Duodenal infusion of donor feces for recurrent Clostridium difficile.The New England Journal of Medicine,368(5):407-415.
Wang Y,Yao WR,Duan JZ,Xu W,Yang GB.2014.Mucosal addressin cell adhesion molecule-1 of rhesus macaques:molecular cloning,expression,and alteration after viral infection.Digestive Diseases and Sciences,59(10):2433-2443.
Yao WR,Yu L,Li D,Yang GB.2017.Molecular cloning and characterization of DNGR-1 in rhesus macaques.Molecular Immunology,87:217-226.
Yu L,Wang FJ,Cui YF,Li D,Yao WR,Yang GB.2018.Molecular characteristics of rhesus macaque interleukin-22:cloning,in vitro expression and biological activities.Immunology,154(4):651-662.
Bauer SA,Arndt TP,Leslie KE,Pearl DL,Turner PY.2011.Obesity in rhesus and cynomolgus macaques:a comparative review of the condition and its implications for research.Comparative Medicine,61(6):514-526.
Bernard NJ.2014.Rheumatoid arthritis:Prevotella copri associated with new-onset untreated RA.Nature Reviews Rheumatology,10(1):2.
Dillon SM,Lee EJ,Kotter CV,Austin GL,Gianella S,Siewe B,Smith DM,Landay AL,Mcmanus MC,Robertson CE,Frank DN,Mccarter MD,Wilson CC.2016.Gut dendritic cell activation links an altered colonic microbiome to mucosal and systemic T-cell activation in untreated HIV-1 infection.Mucosal Immunology,9(1):24-37.
Euler AR,Zurenko GE,Moe JB,Ulrich RG,Yagi Y.1990.Evaluation of two monkey species(Macaca mulatta and Macaca fascicularis)as possible models for human Helicobacter pylori disease.Journal of Clinical Microbiology,28(10):2285-2290.
Feichtinger H,Putkonen P,Parravicini C,Li SL,Kaaya EE,Bottiger D,Biberfeld G,Biberfeld P.1990.Malignant lymphomas in cynomolgus monkeys infected with simian immunodeficiency virus.American Journal of Pathology,137(6):1311-1315.
Kaiko GE,Stappenbeck TS.2014.Host-microbe interactions shaping the gastrointestinal environment.Trends in Immunology,35(11):538-548.
Klatt NR,Harris LD,Vinton CL,Sung H,Briant JA,Tabb B,Morcock D,Mcginty JW,Lifson JD,Lafont BA,Martin MA,Levine AD,Estes JD,Brenchley JM.2010.Compromised gastrointestinal integrity in pigtail macaques is associated with increased microbial translocation,immune activation,and IL-17 production in the absence of SIV infection.Mucosal Immunology,3(4):387-398.
Langille MG,Zaneveld J,Caporaso JG,Mcdonald D,Knights D,Reyes JA,Clemente JC,Burkepile DE,Vega Thurber RL,Knight R,Beiko RG,Huttenhower C.2013.Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences.Nature Biotechnology,31(9):814-821.
Lathrop SK,Bloom SM,Rao SM,Nutsch K,Lio CW,Santacruz N,Peterson DA,Stappenbeck TS,Hsieh CS.2011.Peripheral education of the immune system by colonic commensal microbiota.Nature,478(7368):250-254.
Letvin NL,Daniel MD,Sehgal PK,Desrosiers RC,Hunt RD,Waldron LM,Mackey JJ,Schmidt DK,Chalifoux LV,King NW.1985.Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III.Science,230(4721):71-73.
Li D,Wang FJ,Yu L,Yao WR,Cui YF,Yang GB.2017.Expression of pIgRin the tracheal mucosa of SHIV/SIV-infected rhesus macaques.Zoological Research,38(1):44-48.
Loftin KC,Brown LR,Levy BM.1980.Comparison of the predominant cultivable microflora in the dental plaque of Macaca mulatta(rhesus)and Macaca fascicularis(cynomolgus).Journal of Dental Research,59(10):1606-1612.
Lozupone C,Lladser ME,Knights D,Stombaugh J,Knight R.2011.UniFrac:an effective distance metric for microbial community comparison.The ISMEJournal,5(2):169-172.
Manichanh C,Rigottier-Gois L,Bonnaud E,Gloux K,Pelletier E,Frangeul L,Nalin R,Jarrin C,Chardon P,Marteau P,Roca J,Dore J.2006.Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach.Gut,55(2):205-211.
Niess JH,Adler G.2010.Enteric flora expands gut lamina propria CX3CR1+dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions.Journal of Immunology,184(4):2026-2037.
Parks DH,Tyson GW,Hugenholtz P,Beiko RG.2014.STAMP:statistical analysis of taxonomic and functional profiles.Bioinformatics,30(21):3123-3124.
Rawls JF,Mahowald MA,Ley RE,Gordon JI.2006.Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection.Cell,127(2):423-433.
Reimann KA,Parker RA,Seaman MS,Beaudry K,Beddall M,Peterson L,Williams KE,Veazey RS,Montefiori DC,Mascola JR,Nabel GJ,Letvin NL.2005.Pathogenicity of simian-human immunodeficiency virus SHIV-89.6Pand SIVmac is attenuated in cynomolgus macaques and associated with early T-lymphocyte responses.Journal of Virology,79(14):8878-8885.
Rieder R,Wisniewski PJ,Alderman BL,Campbell SC.2017.Microbes and mental health:A review.Brain,Behavior,and Immunity,66:9-17.
Sokol H,Pigneur B,Watterlot L,Lakhdari O,Bermudez-Humaran LG,Gratadoux JJ,Blugeon S,Bridonneau C,Furet JP,Corthier G,Grangette C,Vasquez N,Pochart P,Trugnan G,Thomas G,Blottiere HM,Dore J,Marteau P,Seksik P,Langella P.2008.Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients.Proceedings of the National Academy of Sciences of the United States of America,105(43):16731-16736.
Stilling RM,Ryan FJ,Hoban AE,Shanahan F,Clarke G,Claesson MJ,Dinan TG,Cryan JF.2015.Microbes&neurodevelopment-Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala.Brain,Behavior,and Immunity,50:209-220.
ten Haaft P,Almond N,Biberfeld G,Cafaro A,Cranage M,Ensoli B,Hunsmann G,Polyanskaya N,Stahl-Hennig C,Thortensson R,Titti F,Heeney J.2001.Comparison of early plasma RNA loads in different macaque species and the impact of different routes of exposure on SIV/SHIVinfection.Journal of Medical Primatology,30(4):207-214.
Tilg H,Moschen AR.2014.Microbiota and diabetes:an evolving relationship.Gut,63(9):1513-1521.
van Nood E,Vrieze A,Nieuwdorp M,Fuentes S,Zoetendal EG,de Vos WM,Visser CE,Kuijper EJ,Bartelsman JF,Tijssen JG,Speelman P,Dijkgraaf MG,Keller JJ.2013.Duodenal infusion of donor feces for recurrent Clostridium difficile.The New England Journal of Medicine,368(5):407-415.
Wang Y,Yao WR,Duan JZ,Xu W,Yang GB.2014.Mucosal addressin cell adhesion molecule-1 of rhesus macaques:molecular cloning,expression,and alteration after viral infection.Digestive Diseases and Sciences,59(10):2433-2443.
Yao WR,Yu L,Li D,Yang GB.2017.Molecular cloning and characterization of DNGR-1 in rhesus macaques.Molecular Immunology,87:217-226.
Yu L,Wang FJ,Cui YF,Li D,Yao WR,Yang GB.2018.Molecular characteristics of rhesus macaque interleukin-22:cloning,in vitro expression and biological activities.Immunology,154(4):651-662.