The strength of gut microbiota transfer along social networks and genealogical lineages in the house mouse

. 2024 May 14 ; 100 (6) : .

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38730559

Grantová podpora
19-19307S Czech Science Foundation
1501218 Charles University
Ministry of Education, Youth and Sports

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.

Zobrazit více v PubMed

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...