The strength of gut microbiota transfer along social networks and genealogical lineages in the house mouse
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články
Grantová podpora
19-19307S
Czech Science Foundation
1501218
Charles University
Ministry of Education, Youth and Sports
PubMed
38730559
PubMed Central
PMC11134300
DOI
10.1093/femsec/fiae075
PII: 7668476
Knihovny.cz E-zdroje
- Klíčová slova
- gastrointestinal tract, inter-individual transmission, microbiome, relatedness, social contact,
- MeSH
- Bacteria genetika klasifikace izolace a purifikace MeSH
- mikrosatelitní repetice MeSH
- myši MeSH
- RNA ribozomální 16S * genetika MeSH
- střevní mikroflóra * genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- myši MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- RNA ribozomální 16S * MeSH
The gut microbiota of vertebrates is acquired from the environment and other individuals, including parents and unrelated conspecifics. In the laboratory mouse, a key animal model, inter-individual interactions are severely limited and its gut microbiota is abnormal. Surprisingly, our understanding of how inter-individual transmission impacts house mouse gut microbiota is solely derived from laboratory experiments. We investigated the effects of inter-individual transmission on gut microbiota in two subspecies of house mice (Mus musculus musculus and M. m. domesticus) raised in a semi-natural environment without social or mating restrictions. We assessed the correlation between microbiota composition (16S rRNA profiles), social contact intensity (microtransponder-based social networks), and mouse relatedness (microsatellite-based pedigrees). Inter-individual transmission had a greater impact on the lower gut (colon and cecum) than on the small intestine (ileum). In the lower gut, relatedness and social contact independently influenced microbiota similarity. Despite female-biased parental care, both parents exerted a similar influence on their offspring's microbiota, diminishing with the offspring's age in adulthood. Inter-individual transmission was more pronounced in M. m. domesticus, a subspecies, with a social and reproductive network divided into more closed modules. This suggests that the transmission magnitude depends on the social and genetic structure of the studied population.
Department of Zoology Faculty of Science Charles University Prague 128 00 Czech Republic
Institute of Animal Physiology and Genetics Czech Academy of Sciences Brno 602 00 Czech Republic
Institute of Vertebrate Biology of the Czech Academy of Sciences Brno 603 00 Czech Republic
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Aitchison J. The Statistical analysis of compositional data. J R Stat Soc Ser B Methodol. 1982;44:139–60.
Amadeu RR, Cellon C, Olmstead JW et al. AGHmatrix: R package to construct relationship matrices for autotetraploid and diploid species: a blueberry example. Plant Genome. 2016;9. 10.3835/plantgenome2016.01.0009. PubMed DOI
Amato KR, Van Belle S, Di Fiore A et al. Patterns in gut microbiota similarity associated with degree of sociality among sex classes of a neotropical primate. Microb Ecol. 2017;74:250–8. PubMed
Bardenhorst SK, Vital M, Karch A et al. Richness estimation in microbiome data obtained from denoising pipelines. Comput Struct Biotechnol J. 2022;20:508–20. PubMed PMC
Bendová B, Mikula O, Vošlajerová Bímová B et al. Divergent gut microbiota in two closely related house mouse subspecies under common garden conditions. FEMS Microbiol Ecol. 2022;98:fiac078. PubMed
Bendová B, Piálek J, Ďureje Ľ et al. How being synanthropic affects the gut bacteriome and mycobiome: comparison of two mouse species with contrasting ecologies. BMC Microbiol. 2020;20:194. PubMed PMC
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.
Beura LK, Hamilton SE, Bi K et al. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature. 2016;532:512–6. PubMed PMC
Callahan BJ, McMurdie PJ, Rosen MJ et al. DADA2: high resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. PubMed PMC
Cekanaviciute E, Yoo BB, Runia TF et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc Natl Acad Sci USA. 2017;114:10713–8. PubMed PMC
Čížková D, Ďureje Ľ, Piálek J et al. Experimental validation of small mammal gut microbiota sampling from faeces and from the caecum after death. Heredity. 2021;127:141–50. PubMed PMC
Čížková D, Schmiedová L, Kváč M et al. The effect of host admixture on wild house mouse gut microbiota is weak when accounting for spatial autocorrelation. Mol Ecol. 2024;33:e17192. PubMed
Debray R, Herbert RA, Jaffe AL et al. Priority effects in microbiome assembly. Nat Rev Micro. 2022;20:109–21. PubMed
den Besten G, van Eunen K, Groen AK et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54:2325–40. PubMed PMC
Dill-McFarland KA, Tang Z-Z, Kemis JH et al. Close social relationships correlate with human gut microbiota composition. Sci Rep. 2019;9:703. PubMed PMC
Dominguez-Bello MG, Costello EK, Contreras M et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010;107:11971–5. PubMed PMC
Ebino KY, Suwa T, Kuwabara Y et al. Lifelong coprophagy in male mice. Exp Anim. 1987;36:273–6. PubMed
Edgar RC. UCHIME2: improved chimera prediction for amplicon sequencing. Biorxiv. 2016;074252. 10.1101/074252. DOI
Ericsson AC, Franklin CL. The gut microbiome of laboratory mice: considerations and best practices for translational research. Mamm Genome. 2021;32:239–50. PubMed PMC
Falush D, Wirth T, Linz B et al. Traces of human migrations in Helicobacter pylori populations. Science. 2003;299:1582–5. PubMed
Ferretti P, Pasolli E, Tett A et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe. 2018;24:133–45.e5. PubMed PMC
Galperin MY, Mekhedov SL, Puigbo P et al. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol. 2012;14:2870–90. PubMed PMC
Graham AL. Naturalizing mouse models for immunology. Nat Immunol. 2021;22:111–7. PubMed
Gresse R, Chaucheyras Durand F, Dunière L et al. Microbiota composition and functional profiling throughout the gastrointestinal tract of commercial weaning piglets. Microorganisms. 2019;7:343. PubMed PMC
Groó Z, Szenczi P, Bánszegi O et al. Natal dispersal in two mice species with contrasting social systems. Behav Ecol Sociobiol. 2013;67:235–42.
Hasan N, Yang H. Factors affecting the composition of the gut microbiota, and its modulation. PeerJ. 2019;7:e7502. PubMed PMC
Hedblom GA, Reiland HA, Sylte MJ et al. Segmented filamentous bacteria—metabolism meets immunity. Front Microbiol. 2018;9:1991. PubMed PMC
Heijtz RD, Wang S, Anuar F et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA. 2011;108:3047–52. PubMed PMC
Hiadlovská Z, Mikula O, Macholán M et al. Shaking the myth: body mass, aggression, steroid hormones, and social dominance in wild house mouse. Gen Comp Endocrinol. 2015;223:16–26. PubMed
Hoffman GE, Schadt EE. variancePartition: interpreting drivers of variation in complex gene expression studies. BMC Bioinf. 2016;17:483. PubMed PMC
Jiang H, Lei R, Ding S-W et al. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinf. 2014;15:182. PubMed PMC
Kalinowski ST, Taper ML, Marshall TC. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol. 2007;16:1099–106. PubMed
Karcher N, Pasolli E, Asnicar F et al. Analysis of 1321 Eubacterium rectale genomes from metagenomes uncovers complex phylogeographic population structure and subspecies functional adaptations. Genome Biol. 2020;21:138. PubMed PMC
Kastl AJ, Terry NA, Wu GD et al. The structure and function of the human small intestinal microbiota: current understanding and future directions. Cell Mol Gastroenterol Hepatol. 2020;9:33–45. PubMed PMC
Kemp KM, Colson J, Lorenz RG et al. Early life stress in mice alters gut microbiota independent of maternal microbiota inheritance. Am J Physiol Regul Integr Comp Physiol. 2021;320:R663–74. PubMed PMC
Kennedy KM, de Goffau MC, Perez-Muñoz ME et al. Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies. Nature. 2023;613:639–49. 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
König B, Markl H. Maternal care in house mice: I. The weaning strategy as a means for parental manipulation of offspring quality. Behav Ecol Sociobiol. 1987;20:1–9.
Kouete MT, Bletz MC, LaBumbard BC et al. Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian. Anim Microbiome. 2023;5:28. PubMed PMC
Kreisinger J, Bastien G, Hauffe HC et al. Interactions between multiple helminths and the gut microbiota in wild rodents. Phil Trans R Soc B. 2015;370:20140295. 10.1098/rstb.2014.0295. PubMed DOI PMC
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;8:50. PubMed PMC
Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest package: tests in linear mixed effects models. J Stat Soft. 2017;82:1–26.
Latham N, Mason G. From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory. Appl Anim Behav Sci. 2004;86:261–89.
Lax S, Smith DP, Hampton-Marcell J et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345:1048–52. PubMed PMC
Legendre P, Legendre L. Numerical ecology. Elsevier, 1998, 852.
Li H, Li T, Yao M et al. Pika gut may select for rare but diverse environmental bacteria. Front Microbiol. 2016;7:1269. PubMed PMC
Linz B, Balloux F, Moodley Y et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature. 2007;445:915–8. PubMed PMC
Louis P, Solvang M, Duncan SH et al. Dietary fibre complexity and its influence on functional groups of the human gut microbiota. Proc Nutr Soc. 2021;80:386–97.
Manfredo Vieira S, Hiltensperger M, Kumar V et al. Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science. 2018;359:1156–61. PubMed PMC
Mikula O, Macholán M, Ďureje Ľ et al. House mouse subspecies do differ in their social structure. Ecol Evol. 2022;12:e9683. PubMed PMC
Moeller AH, Caro-Quintero A, Mjungu D et al. Cospeciation of gut microbiota with hominids. Science. 2016;353:380–2. PubMed PMC
Moeller AH, Foerster S, Wilson ML et al. Social behavior shapes the chimpanzee pan-microbiome. Sci Adv. 2016;2:e1500997. PubMed PMC
Moeller AH, Suzuki TA, Phifer-Rixey M et al. Transmission modes of the mammalian gut microbiota. Science. 2018;362:453–7. PubMed
Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 2008;42:165–90. PubMed
Moudra A, Niederlova V, Novotny J et al. Phenotypic and clonal stability of antigen-inexperienced memory-like T cells across the genetic background, hygienic status, and aging. J Immunol. 2021;206:2109–21. PubMed PMC
Oksanen F, Simpson G, Blanchet F et al. vegan: Community Ecology Package. R package: Version. 2020, 2.3. https://cran.r-project.org/web/packages/vegan/index.html.
Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–8. PubMed
Perez-Muñoz ME, Arrieta M-C, Ramer-Tait AE et al. A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome. Microbiome. 2017;5:48. 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:D590–6. PubMed PMC
Raulo A, Allen BE, Troitsky T et al. Social networks strongly predict the gut microbiota of wild mice. ISME J. 2021;15:2601–13. 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.e13. PubMed PMC
Roswall J, Olsson LM, Kovatcheva-Datchary P et al. Developmental trajectory of the healthy human gut microbiota during the first 5 years of life. Cell Host Microbe. 2021;29:765–76. PubMed
Sarkar A, Harty S, Johnson KV-A et al. Microbial transmission in animal social networks and the social microbiome. Nat Ecol Evol. 2020;4:1020–35. PubMed
Stearns JC, Lynch MDJ, Senadheera DB et al. Bacterial biogeography of the human digestive tract. Sci Rep. 2011;1:170. PubMed PMC
Suzuki TA, Fitzstevens JL, Schmidt VT et al. Codiversification of gut microbiota with humans. Science. 2022;377:1328–32. PubMed PMC
Suzuki TA, Nachman MW. Spatial heterogeneity of gut microbial composition along the gastrointestinal tract in natural populations of house mice. PLoS One. 2016;11:e0163720. PubMed PMC
Těšický M, Schmiedová L, Krajzingrová T et al. Nearly (?) sterile avian egg in a passerine bird. FEMS Microbiol Ecol. 2024;100:fiad164. PubMed PMC
Tung J, Barreiro LB, Burns MB et al. Social networks predict gut microbiome composition in wild baboons. eLife. 2015;4:e05224. PubMed PMC
Valles-Colomer M, Blanco-Míguez A, Manghi P et al. The person-to-person transmission landscape of the gut and oral microbiomes. Nature. 2023;614:125–35. PubMed PMC
van den Boogaart KG, Tolosana-Delgado R. “Compositions”: a unified R package to analyze compositional data. Comput Geosci. 2008;34:320–38.
van den Elsen LWJ, Garssen J, Burcelin R et al. Shaping the gut microbiota by breastfeeding: the gateway to allergy prevention?. Front Pediatr. 2019;7:47. PubMed PMC
van Paridon JP, Bolker B, Alday P. lmerMultiMember: Multiple membership random effects. 2022. https://jvparidon.github.io/lmerMultiMember/ (25 June 2023, date last accessed).
van Zegeren K. Variation in aggressiveness and the regulation of numbers in house mouse populations. Neth J Zool. 1979;30:635–770.
Vemuri R, Shankar EM, Chieppa M et al. Beyond just bacteria: functional biomes in the gut ecosystem including virome, mycobiome, archaeome and helminths. Microorganisms. 2020;8:483. PubMed PMC
Wang Q, Garrity GM, Tiedje JM et al. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb. 2007;73:5261–7. PubMed PMC
Wang S, Ryan CA, Boyaval P et al. Maternal vertical transmission affecting early-life microbiota development. Trends Microbio. 2020;28:28–45. PubMed
Warton DI, Hui FK. The arcsine is asinine: the analysis of proportions in ecology. Ecology. 2011;92:3–10. PubMed
Wasimuddin, Cizkova D, Bryja J et al. High prevalence and species diversity of Helicobacter spp. detected in wild house mice. Appl Environ Microb. 2012;78:8158–60. PubMed PMC
Waskito LA, Yamaoka Y. The story of Helicobacter pylori: depicting human migrations from the phylogeography. Adv Exp Med Biol. 2019;1149:1–16. PubMed
Wernroth M-L, Peura S, Hedman AM et al. Development of gut microbiota during the first 2 years of life. Sci Rep. 2022;12:9080. PubMed PMC
White J, Mirleau P, Danchin E et al. Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. Ecol Lett. 2010;13:1515–24. PubMed PMC
Zoetendal EG, Raes J, van den Bogert B et al. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 2012;6:1415–26. PubMed PMC