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Geographical location influences the composition of the gut microbiota in wild house mice (Mus musculus domesticus) at a fine spatial scale


Autoři: Sarah Goertz aff001;  Alexandre B. de Menezes aff002;  Richard J. Birtles aff003;  Jonathan Fenn aff001;  Ann E. Lowe aff001;  Andrew D. C. MacColl aff001;  Benoit Poulin aff001;  Stuart Young aff004;  Janette E. Bradley aff001;  Christopher H. Taylor aff001
Působiště autorů: School of Life Sciences, University of Nottingham, Nottingham, United Kingdom aff001;  School of Natural Sciences, NUI Galway, Galway, Ireland aff002;  School of Environment and Life Sciences, University of Salford, Manchester, United Kingdom aff003;  IUCN SSC Asian Wild Cattle Specialist Group, c/o Chester Zoo, Chester, United Kingdom aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222501

Souhrn

The composition of the mammalian gut microbiota can be influenced by a multitude of environmental variables such as diet and infections. Studies investigating the effect of these variables on gut microbiota composition often sample across multiple separate populations and habitat types. In this study we explore how variation in the gut microbiota of the house mouse (Mus musculus domesticus) on the Isle of May, a small island off the east coast of Scotland, is associated with environmental and biological factors. Our study focuses on the effects of environmental variables, specifically trapping location and surrounding vegetation, as well as the host variables sex, age, body weight and endoparasite infection, on the gut microbiota composition across a fine spatial scale in a freely interbreeding population. We found that differences in gut microbiota composition were significantly associated with the trapping location of the host, even across this small spatial scale. Sex of the host showed a weak association with microbiota composition. Whilst sex and location could be identified as playing an important role in the compositional variation of the gut microbiota, 75% of the variation remains unexplained. Whereas other rodent studies have found associations between gut microbiota composition and age of the host or parasite infections, the present study could not clearly establish these associations. We conclude that fine spatial scales are important when considering gut microbiota composition and investigating differences among individuals.

Klíčová slova:

Gut bacteria – Islands – Microbiome – Parasitic diseases – Rodents – Trophic interactions – Clostridium – Shannon index


Zdroje

1. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G. Environmental and gut Bacteroidetes: The food connection. Front Microbiol. 2011; doi: 10.3389/fmicb.2011.00093 21747801

2. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009; doi: 10.1038/nri2515 19343057

3. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013; doi: 10.1038/nature12331 23842501

4. Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD, Shanahan F, et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry.; 2013; doi: 10.1038/mp.2012.77 22688187

5. Langille MGI, Meehan CJ, Koenig JE, Dhanani AS, Rose RA, Howlett SE, et al. Microbial shifts in the aging mouse gut. Microbiome. 2014; doi: 10.1186/s40168-014-0050-9 25520805

6. Holm JB, Sorobetea D, Kiilerich P, Ramayo-Caldas Y, Estellé J, Ma T, et al. Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of Lactobacilli. PLoS One. 2015; doi: 10.1371/journal.pone.0125495 25942314

7. Dominianni C, Sinha R, Goedert JJ, Pei Z, Yang L, Hayes RB, et al. Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLoS One. 2015; doi: 10.1371/journal.pone.0124599 25874569

8. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci. 2010; doi: 10.1073/pnas.1007028107 20937875

9. Bonder MJ, Kurilshikov A, Tigchelaar EF, Mujagic Z, Imhann F, Vila AV, et al. The effect of host genetics on the gut microbiome. Nat Genet. 2016; doi: 10.1038/ng.3663 27694959

10. Vaishampayan PA, Kuehl J V., Froula JL, Morgan JL, Ochman H, Francino MP. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol. 2010; doi: 10.1093/gbe/evp057 20333224

11. Tannock GW, Fuller R, Smith SL, Hall MA. Plasmid profiling of members of the family Enterobacteriaceae, Lactobacilli, and Bifidobacteria to study the transmission of bacteria from mother to infant. J Clin Microbiol. 1990;28,6:1225–8. 2380352

12. Thompson CL, Wang B, Holmes AJ. The immediate environment during postnatal development has long-term impact on gut community structure in pigs. ISME J. 2008; doi: 10.1038/ismej.2008.29 18356821

13. Weldon L, Abolins S, Lenzi L, Bourne C, Riley EM, Viney M. The gut microbiota of wild mice. PLoS One. 2015; doi: 10.1371/journal.pone.0134643 26258484

14. Linnenbrink M, Wang J, Hardouin EA, Künzel S, Metzler D, Baines JF. The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol Ecol. 2013; doi: 10.1111/mec.12206 23398547

15. Suzuki TA, Martins FM, Nachman MW. Altitudinal variation of the gut microbiota in wild house mice. Mol Ecol. 2018; doi: 10.1111/mec.14905 30346069

16. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012; doi: 10.1038/nature11053 22699611

17. 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; doi: 10.1111/mec.12909 25204516

18. Amato KR, Martinez-Mota R, Righini N, Raguet-Schofield M, Corcione FP, Marini E, et al. Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species. Oecologia.; 2016; doi: 10.1007/s00442-015-3507-z 26597549

19. Wang J, Linnenbrink M, Künzel S, Fernandes R, Nadeau M-J, Rosenstiel P, et al. Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. Proc Natl Acad Sci. 2014; doi: 10.1073/pnas.1402342111 24912178

20. Hildebrand F, Nguyen TLA, Brinkman B, Yunta RG, Cauwe B, Vandenabeele P, et al. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 2013; doi: 10.1186/gb-2013-14-1-r4 23347395

21. Org E, Mehrabian M, Parks BW, Shipkova P, Liu X, Drake TA, et al. Sex differences and hormonal effects on gut microbiota composition in mice. Gut Microbes; 2016; doi: 10.1080/19490976.2016.1203502 27355107

22. Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E, Parks B, et al. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun. 2014; doi: 10.1038/ncomms5500 25072318

23. Yurkovetskiy L, Burrows M, Khan AA, Graham L, Volchkov P, Becker L, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity.; 2013; doi: 10.1016/j.immuni.2013.08.013 23973225

24. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011; doi: 10.1038/nature09944 21508958

25. Snijders AM, Langley SA, Kim Y-M, Brislawn CJ, Noecker C, Zink EM, et al. Influence of early life exposure, host genetics and diet on the mouse gut microbiome and metabolome. Nat Microbiol. 2016; doi: 10.1038/nmicrobiol.2016.221 27892936

26. McKenney EA, Williamson L, Yoder AD, Rawls JF, Bilbo SD, Parker W. Alteration of the rat cecal microbiome during colonization with the helminth Hymenolepis diminuta. Gut Microbes. 2015; doi: 10.1080/19490976.2015.1047128 25942385

27. Walk ST, Blum AM, Ewing SA-S, Weinstock J V., Young VB. Alteration of The Murine Gut Microbiota During Infection with the parasitic helminth, Heligmosomoides polygyrus. Inflamm Bowel Dis. 2010; doi: 10.1002/ibd.21299 20848461

28. Reynolds LA, Finlay BB, Maizels RM. Cohabitation in the Intestine: Interactions among Helminth Parasites, Bacterial Microbiota, and Host Immunity. J Immunol. 2015; doi: 10.4049/jimmunol.1501432 26477048

29. Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos Trans R Soc B Biol Sci. 2015; doi: 10.1098/rstb.2014.0295 26150661

30. Berry RJ. The Evolution of an Island Population of the House Mouse. Source Evol. 1964; doi: 10.1111/j.1558-5646.1964.tb01623.x

31. Triggs GS. The population ecology of house mice (Mus domesticus) on the Isle of May, Scotland. J Zool. 1991; doi: 10.1111/j.1469-7998.1991.tb03828.x

32. Berry RJ, Triggs GS, King P, Nash HR, Noble LR. Hybridization and gene flow in house mice introduced into an existing population on an island. J Zool. 1991; doi: 10.1111/j.1469-7998.1991.tb04329.x

33. Berry RJ. House Mouse Mus domesticus. Handbook of British Mammals. Corbet GB, Harris S, editors. Handbook of British Mammals. 1991. 239–247.

34. Taylor CH, Young S, Fenn J, Lamb AL, Lowe AE, Poulin B, et al. Immune state is associated with natural dietary variation in wild mice Mus musculus domesticus. Funct Ecol. 2019; doi: 10.1111/1365-2435.13354

35. Kettel EF, Perrow MR, Reader T. Live-trapping in the stalk zone of tall grasses as an effective way of monitoring harvest mice (Micromys minutus). Eur J Wildl Res. 2016; doi: 10.1007/s10344-016-0985-1

36. Rowe F, Bradfield A, Quy R, Swinney T. Relationship Between Eye Lens Weight and Age in the Wild House Mouse (Mus musculus). J Appl Ecol. 1985; doi: 22.55.10.2307/2403326

37. Augusteyn RC. Growth of the eye lens: I. Weight accumulation in multiple species. Mol Vis. 2014;20:410–26. 24715758

38. Carreno NB, Brigada AM, Rosi MI, Castro-Vazquez A. Estimating Ages of Corn Mice (Calomys musculinus). J Mammal. 1990; doi: 10.2307/1381964

39. Abolins S, King EC, Lazarou L, Weldon L, Hughes L, Drescher P, et al. The comparative immunology of wild and laboratory mice, Mus musculus domesticus. Nat Commun. 2017; doi: 10.1038/ncomms14811 28466840

40. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS. 2011; doi: 10.1073/pnas.1000080107 20534432

41. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; doi: 10.1093/bioinformatics/btr381 21700674

42. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009; doi: 10.1128/AEM.01541-09 19801464

43. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013; doi: 10.1093/nar/gks1219 23193283

44. Andrews S. FastQC: a quality control tool for high throughput sequence data. 2010. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc.

45. Bushnell B, Rood J, Singer E. BBMerge–Accurate paired shotgun read merging via overlap. PLoS One. 2017; doi: 10.1371/journal.pone.0185056 29073143

46. McMurdie PJ, Holmes S. Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS One. 2013; doi: 10.1371/journal.pone.0061217 23630581

47. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, Hara RBO, et al. Package ‘vegan’ version 2.3–1. 2015. Available online at: https://www.cran.r-project.org/web/packages/vegan/vegan.pdf.

48. McMurdie PJ, Holmes S. Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible. PLoS Comput Biol. 2014; doi: 10.1371/journal.pcbi.1003531 24699258

49. Schulte-Hostedde AI, Millar JS, Hickling GJ. Evaluating body condition in small mammals. Can J Zool. 2011; doi: 10.1139/z01-073

50. Lozupone C, Knight R, Lozupone C, Knight R. UniFrac: a New Phylogenetic Method for Comparing Microbial Communities. Appl Environ Microbiol. 2005; doi: 10.1128/AEM.71.12.8228–8235.2005

51. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001; doi: 10.1111/j.1442-9993.2001.01070.pp.x

52. Love AM, Anders S, Huber W, Love MM. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Available online at: https://www.github.com/mikelove/DESeq2.

53. Maurice CF, Cl Knowles S, Ladau J, Pollard KS, Fenton A, Pedersen AB, et al. Marked seasonal variation in the wild mouse gut microbiota. ISME J. 2015; doi: 10.1038/ismej.2015.53 26023870

54. Biddle A, Stewart L, Blanchard J, Leschine S. Untangling the genetic basis of fibrolytic specialization by lachnospiraceae and ruminococcaceae in diverse gut communities. Diversity. 2013; doi: 10.3390/d5020374

55. Suzuki TA, Phifer-Rixey M, Mack KL, Sheehan MJ, Lin D, Bi K, et al. Host genetic determinants of the gut microbiota of wild mice. Mol Ecol. 2019; doi: 10.1111/mec.15139 31141224

56. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: Potential for new insights from genomic analysis. Nat Rev Microbiol. 2008; doi: 10.1038/nrmicro1817 18180751

57. Rogers GB, Kozlowska J, Keeble J, Metcalfe K, Fao M, Dowd SE, et al. Functional divergence in gastrointestinal microbiota in physically-separated genetically identical mice. Sci Rep. 2014; doi: 10.1038/srep05437 24961643

58. Kotzampassi K, Giamarellos-bourboulis EJ, Stavrou G. Bacteria and Obesity: The Proportion Makes the Difference. Surg Curr Res. 2013; doi: 10.4172/2161-1076.1000152

59. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the Human Intestinal Microbial Flora. Science. 2005; doi: 10.1126/science.1110591 15831718

60. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci. 2010; doi: 10.1073/pnas.1007028107 20937875

61. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; doi: 10.1371/journal.pbio.0050177 17594176

62. Li H, Li T, Beasley DAE, Heděnec P, Xiao Z, Zhang S, et al. Diet diversity is associated with beta but not alpha diversity of pika gut microbiota. Front Microbiol. 2016; doi: 10.3389/fmicb.2016.01169 27512391

63. Markle JGM, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, et al. Sex Differences in the Gut. Science. 2013; doi: 10.5534/wjmh.190009 30929328

64. Hayes KS, Bancroft AJ, Goldrick M, Portsmouth C, Roberts IS, Grencis RK. Exploitation of the Intestinal Microflora by the Parasitic Nematode Trichuris muris. Science. 2010; doi: 10.1126/science.1187703 20538949

65. Vandeputte D, Kathagen G, D’hoe K, Vieira-Silva S, Valles-Colomer M, Sabino J, et al. Quantitative Microbiome profiling links gut community variation to microbial load. Nature. 2017; doi: 10.1038/nature24460 29143816


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