How being synanthropic affects the gut bacteriome and mycobiome: comparison of two mouse species with contrasting ecologies
Language English Country Great Britain, England Media electronic
Document type Comparative Study, Journal Article, Research Support, Non-U.S. Gov't
Grant support
18-17796Y
Grantová Agentura České Republiky - International
1501218
Grantová Agentura, Univerzita Karlova (CZ) - International
PubMed
32631223
PubMed Central
PMC7336484
DOI
10.1186/s12866-020-01859-8
PII: 10.1186/s12866-020-01859-8
Knihovny.cz E-resources
- Keywords
- Evolution, Metabarcoding, Microbiome, Muridae, Steppe mouse, Symbiosis,
- MeSH
- Bacteria classification genetics isolation & purification MeSH
- Ecology MeSH
- Feces microbiology MeSH
- Phylogeny MeSH
- Fungi classification genetics isolation & purification MeSH
- Microbiota MeSH
- Mycobiome MeSH
- Mice MeSH
- DNA, Ribosomal genetics MeSH
- RNA, Ribosomal, 16S genetics MeSH
- Sequence Analysis, DNA methods MeSH
- High-Throughput Nucleotide Sequencing MeSH
- Animals MeSH
- Check Tag
- Mice MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Comparative Study MeSH
- Names of Substances
- DNA, Ribosomal MeSH
- RNA, Ribosomal, 16S MeSH
BACKGROUND: The vertebrate gastrointestinal tract is colonised by microbiota that have a major effect on the host's health, physiology and phenotype. Once introduced into captivity, however, the gut microbial composition of free-living individuals can change dramatically. At present, little is known about gut microbial changes associated with adaptation to a synanthropic lifestyle in commensal species, compared with their non-commensal counterparts. Here, we compare the taxonomic composition and diversity of bacterial and fungal communities across three gut sections in synanthropic house mouse (Mus musculus) and a closely related non-synanthropic mound-building mouse (Mus spicilegus). RESULTS: Using Illumina sequencing of bacterial 16S rRNA amplicons, we found higher bacterial diversity in M. spicilegus and detected 11 bacterial operational taxonomic units with significantly different proportions. Notably, abundance of Oscillospira, which is typically higher in lean or outdoor pasturing animals, was more abundant in non-commensal M. spicilegus. ITS2-based barcoding revealed low diversity and high uniformity of gut fungi in both species, with the genus Kazachstania clearly dominant. CONCLUSIONS: Though differences in gut bacteria observed in the two species can be associated with their close association with humans, changes due to a move from commensalism to captivity would appear to have caused larger shifts in microbiota.
CBGP Montpellier SupAgro INRA CIRAD IRD Univ Montpellier Montferrier sur Lez France
Department of Zoology Faculty of Science Charles University Prague Czech Republic
See more in PubMed
Cucchi T, Auffray J-C, Vigne J-D. On the origin of the house mouse synanthropy and dispersal in the near east and Europe: zooarcheological review and perspectives. In: Macholan M, Baird SJE, Munclinger P, Pialek J, editors. Evolution of the House Mouse. Cambridge: Cambridge University Press; 2012. pp. 65–93.
Driscoll CA, Macdonald DW, O’Brien SJ. From wild animals to domestic pets, an evolutionary view of domestication. Proc Natl Acad Sci. 2009;106:9971–9978. PubMed PMC
Hu Y, Hu S, Wang W, et al. Earliest evidence for commensal processes of cat domestication. Proc Natl Acad Sci. 2014;111:116–120. PubMed PMC
Shapira I, Sultan H, Shanas U. Agricultural farming alters predator-prey interactions in nearby natural habitats. Anim Conserv. 2008;11:1–8.
Morgan M. Methicillin-resistant Staphylococcus aureus and animals: zoonosis or humanosis? J Antimicrob Chemother. 2008;62:1181–1187. PubMed
Hendry AP, Farrugia TJ, Kinnison MT. Human influences on rates of phenotypic change in wild animal populations. Mol Ecol. 2008;17:20–29. PubMed
Hemmer H. Domestication: the decline of environmental appreciation. Cambridge: Cambridge University Press; 1990.
O’Connor TP. Working at relationships: another look at animal domestication. Antiquity. 1997;71:149–156.
Leach HM. Human domestication reconsidered. Curr Anthropol. 2003;44:349–368.
Dobney K, Larson G. Genetics and animal domestication: new windows on an elusive process. J Zool. 2006;269:060222013030001–060222013030???.
Varudkar A, Ramakrishnan U. Gut microflora may facilitate adaptation to anthropic habitat: a comparative study in Rattus. Ecol Evol. 2018;8:6463–6472. PubMed PMC
Sekirov I, Russell SL, Antunes LCM, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90:859–904. PubMed
Wallace TC, Guarner F, Madsen K, et al. Human gut microbiota and its relationship to health and disease. Nutr Rev. 2011;69:392–403. PubMed
Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13:260–270. PubMed PMC
Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–1031. PubMed
Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701–712. PubMed
Häcker G, Redecke V, Häcker H. Activation of the immune system by bacterial CpG-DNA. Immunology. 2002;105:245–251. PubMed PMC
Tlaskalová-Hogenová H, Štěpánková R, Hudcovic T, et al. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett. 2004;93:97–108. PubMed
Round JL. Shaping up with the gut microbiota. Sci Transl Med. 2014;6:263ec201.
Taylor KD, Strom SP, Funari VA, et al. Interactions between commensal Fungi and the C-type Lectin receptor Dectin-1 influence colitis. Science. 2012;336:1314–1317. PubMed PMC
Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized Gnotobiotic mice. Sci Transl Med. 2009;1:6ra14. PubMed PMC
Walk ST, Blum AM, Ewing SA-S, et al. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm Bowel Dis. 2010;16:1841–1849. PubMed PMC
Heisel T, Montassier E, Johnson A, et al. High-fat diet changes fungal microbiomes and Interkingdom relationships in the murine gut. mSphere. 2017;2:1–14. PubMed PMC
Dhanasiri AKS, Brunvold L, Brinchmann MF, et al. Changes in the intestinal microbiota of wild Atlantic cod Gadus morhua L. upon captive rearing. Microb Ecol. 2011;61:20–30. PubMed
Kohl KD, Dearing MD. Wild-caught rodents retain a majority of their natural gut microbiota upon entrance into captivity. Environ Microbiol Rep. 2014;6:191–195. PubMed
Metcalf JL, Song SJ, Morton JT, et al. Evaluating the impact of domestication and captivity on the horse gut microbiome. Sci Rep. 2017;7:1–9. PubMed PMC
McKenzie VJ, Kowalewski M, Di Fiore A, et al. The effects of captivity on the mammalian gut microbiome. Integr Comp Biol. 2017;57:690–704. PubMed PMC
Aplin KP, Suzuki H, Chinen AA, et al. Multiple geographic origins of commensalism and complex dispersal history of black rats. PLoS One. 2011;6:e26357. PubMed PMC
Ohnishi N, Yuasa H, Tanaka S, et al. Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci. 2008;105:1003–1008. PubMed PMC
Kau AL, Ahern PP, Griffin NW, et al. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474:327–336. PubMed PMC
Iliev ID, Funari VA, Taylor KD, et al. Interactions between commensal Fungi and the C-type Lectin receptor Dectin-1 influence colitis. Science. 2012;336:1314–1317. PubMed PMC
Gu S, Chen D, Zhang J-NN, et al. Bacterial community mapping of the mouse gastrointestinal tract. PLoS One. 2013;8:e74957. PubMed PMC
Linnenbrink M, Wang J, Hardouin EA, et al. The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol Ecol. 2013;22:1904–1916. PubMed
Kreisinger J, Čížková D, Vohánka J, Piálek J. Gastrointestinal microbiota of wild and inbred individuals of two house mouse subspecies assessed using high-throughput parallel pyrosequencing. Mol Ecol. 2014;23:5048–5060. PubMed
Suzuki TA, Nachman MW. Spatial heterogeneity of gut microbial composition along the gastrointestinal tract in natural populations of house mice. PLoS One. 2016;11:1–15. PubMed PMC
Kreisinger J, Bastien G, Hauffe HC, et al. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos Trans R Soc B Biol Sci. 2015;370:20140295. PubMed PMC
Siriyappagouder P, Kiron V, Lokesh J, et al. The intestinal Mycobiota in wild Zebrafish comprises mainly Dothideomycetes while Saccharomycetes predominate in their laboratory-reared counterparts. Front Microbiol. 2018;9:1–13. PubMed PMC
Sarver B, Keeble S, Cosart T, Tucker PK, Dean MD, Good JM. Phylogenomic insights into mouse evolution using a pseudoreference approach. Genome Biol Evol. 2017;9:726–739. doi: 10.1093/gbe/evx034. PubMed DOI PMC
Sokolov VE, Kotenkova EV, Michailenko AG. Mus spicilegus. Mamm Species. 1998;592:1–6.
Kreisinger J, Kropáčková L, Petrželková A, et al. Temporal stability and the effect of Transgenerational transfer on fecal microbiota structure in a long distance migratory bird. Front Microbiol. 2017;8:1–19. PubMed PMC
Scupham AJ, Patton TG, Bent E, Bayles DO. Comparison of the Cecal microbiota of domestic and wild turkeys. Microb Ecol. 2008;56:322–331. PubMed
Clayton JB, Vangay P, Huang H, et al. Captivity humanizes the primate microbiome. Proc Natl Acad Sci. 2016;113:10376–10381. PubMed PMC
Rosshart SP, Vassallo BG, Angeletti D, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. 2017;171:1015–1028.e13. PubMed PMC
Kohl KD, Skopec MM, Dearing MD. Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conserv Physiol. 2014;2:1–11. PubMed PMC
Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012;9:577–589. PubMed
Lu H-P, Lai Y-C, Huang S-W, et al. Spatial heterogeneity of gut microbiota reveals multiple bacterial communities with distinct characteristics. Sci Rep. 2015;4:6185. PubMed PMC
Mackie RI, Aminov RI, Hu W, et al. Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches. Appl Environ Microbiol. 2003;69:6808–6815. PubMed PMC
Konikoff T, Gophna U. Oscillospira: a central, enigmatic component of the human gut microbiota. Trends Microbiol. 2016;24:523–524. PubMed
Gophna U, Konikoff T, Nielsen HB. Oscillospira and related bacteria–from metagenomic species to metabolic features. Environ Microbiol. 2017;19:835–841. PubMed
Gomez-Arango LF, Barrett HL, McIntyre HD, et al. Increased systolic and diastolic blood pressure is associated with altered gut microbiota composition and butyrate production in early pregnancy. Hypertension. 2016;68:974–981. PubMed
Noble EE, Hsu TM, Kanoski SE. Gut to brain Dysbiosis: mechanisms linking Western diet consumption, the microbiome, and cognitive impairment. Front Behav Neurosci. 2017;11:1–10. PubMed PMC
Wasimuddin ČD, Bryja J, et al. High prevalence and species diversity of helicobacter spp. detected in wild house mice. Appl Environ Microbiol. 2012;78:8158–8160. PubMed PMC
Ding S-ZSZ, Minohara Y, Xue JF, et al. Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun. 2007;75:4030–4039. PubMed PMC
Linz B, Balloux F, Moodley Y, et al. An African origin for the intimate association between humans and helicobacter pylori. Nature. 2007;445:915–918. PubMed PMC
Atherton JC, Blaser MJ. Coadaptation of helicobacter pylori and humans: ancient history, modern implications. J Clin Invest. 2009;119:2475–2487. PubMed PMC
Kurtzman CP, Robnett CJ, Ward JM, et al. Multigene phylogenetic analysis of pathogenic Candida species in the Kazachstania (Arxiozyma) telluris complex and description of their ascosporic states as Kazachstania bovina sp. nov., K. heterogenica sp. nov., K. pintolopesii sp. nov., and K. slooffiae. J Clin Microbiol. 2005;43:101–111. PubMed PMC
Urubschurov V, Janczyk P, Souffrant W-B, et al. Establishment of intestinal microbiota with focus on yeasts of unweaned and weaned piglets kept under different farm conditions. FEMS Microbiol Ecol. 2011;77:493–502. PubMed
Urubschurov V, Büsing K, Freyer G, et al. New insights into the role of the porcine intestinal yeast, Kazachstania slooffiae, in intestinal environment of weaned piglets. FEMS Microbiol Ecol. 2017;93:1–12. PubMed
Flahou B, De Baere T, Chiers K, et al. Gastric infection with kazachstania heterogenica influences the outcome of a helicobacter suis infection in mongolian gerbils. Helicobacter. 2010;15:67–75. PubMed
Alvarez-Perez S, Mateos A, Dominguez L, et al. First isolation of the anamorph of Kazachstania heterogenica from a fatal infection in a primate host. Med Mycol. 2012;50:193–196. PubMed
Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, Casey CA, Thompson EA, Fraser KA, Rosato PC, Filali-Mouhim A, Sekaly RP, Jenkins MK, Vezys V, Haining WN, Jameson SC, Masopust D. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature. 2016;532:512–516. PubMed PMC
Klindworth A, Pruesse E, Schweer T, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1. PubMed PMC
White T, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. New York: Academic Press Inc; 1990. pp. 315–322.
Jiang H, Lei R, Ding S-W, et al. Skewer: a fast and accurate adapter trimmer for next-generation sequencing pairedend reads. BMC Bioinformatics. 2014;15:1–12. PubMed PMC
Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–583. PubMed PMC
Edgar RC, Haas BJ, Clemente JC, et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200. PubMed PMC
Kõljalg U, Nilsson RH, Abarenkov K, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22:5271–5277. PubMed
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naıve Bayesian classifier for rapid assignment of rRNA sequences. Appl Environ Microbiol. 2007;73:5261–5267. PubMed PMC
DeSantis TZ, Hugenholtz P, Larsen N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–5072. PubMed PMC
Caporaso JG, Bittinger K, Bushman FD, et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26:266–267. PubMed PMC
Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26:1641–1650. PubMed PMC
McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8:e61217. PubMed PMC
Crawley MJ. The R book. New York: Wiley Publishing; 2007.
Yi N, Liu N, Zhi D, Li J. Hierarchical generalized linear models for multiple groups of rare and common variants: jointly estimating group and individual-variant effects. PLoS Genet. 2011;7:e1002382. PubMed PMC
Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci. 2003;100:9440–9445. PubMed PMC
Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–596. PubMed PMC
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–780. PubMed PMC
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. PubMed PMC