bioRxiv Science⌕ Search

Biology subjects

Knowles, S. C.

Publications and source records attributed to Knowles, S. C..

3 recordsLinked to original sources

Social and environmental transmission spread different sets of gut microbes in wild mice

Gut microbes shape many aspects of organismal biology, yet how these key bacteria transmit among hosts in natural populations remains poorly understood. Recent work in mammals has emphasized either transmission through social contacts or indirect transmission through environmental contact, but the relative importance of different routes has not been directly assessed. Here, we used a novel RFID-based tracking system to collect long-term high resolution data on social relationships, space use and microhabitat in a wild population of mice (Apodemus sylvaticus), while regularly characterising their gut microbiota. Through probabilistic modelling of the resulting data, we identify positive and statistically distinct signals of social and environmental transmission, captured by social networks and overlap in home ranges respectively. Strikingly, microbes with distinct biological attributes drove these different transmission signals. While aerotolerant spore-forming bacteria drove the effect of shared space use, a mix of taxa but especially anaerobic bacteria underpinned the social networks effect on gut microbiota similarity. These findings provide the first evidence for parallel social and environmental transmission of gut microbes that involve biologically distinct subsets of the mammalian gut microbiota. List of contributionsO_LIAura Raulo designed the study, helped develop the new RFID tracking technology, collected the data from Wytham, completed all laboratory analyses on gut microbiota profiling prior to sequencing, developed analytical methods, analysed the data and wrote the manuscript C_LIO_LIPaul Burkner helped design the Bayesian probabilistic modeling framework and provided feedback on the manuscript C_LIO_LIJarrah Dale helped collect field data using RFID loggers C_LIO_LIHolly English helped collect field data using RFID loggers and provided feedback on home range analyses C_LIO_LIGenevieve Finerty helped with home range analysis and the analysis of microhabitat variation and provided feedback on the manuscript C_LIO_LICurt Lamberth led development of RFID tracking devices and helped collect field data from Wytham C_LIO_LIJosh Firth supervised the research project, developed social network analysis methods and provided feedback on the analyses and the manuscript C_LIO_LITim Coulson supervised the research project and provided feedback on the analyses and the manuscript C_LIO_LISarah Knowles supervised the research project, helped develop the tracking technology and design the study, collected data from Wytham, planned and supervised laboratory methods, developed analytical methods and provided feedback on analyses and the manuscript. C_LI

ecology↗

Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice

The mammalian gut microbiota influences a wide array of phenotypes and is considered a key determinant of fitness, yet knowledge about the transmission routes by which gut microbes colonise hosts in natural populations remains limited. Here, we use an intensively studied wild population of wood mice (Apodemus sylvaticus) to examine how vertical (maternal) and horizontal (social) transmission routes influence gut microbiota composition throughout life. We identify independent signals of maternal transmission (sharing of taxa between a mother and her offspring) and social transmission (sharing of taxa predicted by the social network), whose relative magnitudes shift as hosts age. In early life, gut microbiota composition is predicted to a similar extent by both maternal and social relationships, but by adulthood the impact of maternal transmission becomes undetectable, leaving only a signal of social transmission. By exploring which taxa drive the maternal transmission signal, we further identify a candidate maternally-transmitted bacterial family in wood mice, the Lactobacillaceae. Overall, our findings suggest a shifting transmission landscape for wild mice, with a mothers influence on microbiota composition waning as offspring age, while the impact of social contacts remains strong and consistent.

microbiology↗

Bifidobacterium castoris strains isolated from wild mice show evidence of frequent host switching and diverse carbohydrate metabolism potential

Members of the gut microbiota genus Bifidobacterium are widely distributed human and animal symbionts believed to exert beneficial effects on their hosts. However, in-depth genomic analyses of animal-associated species and strains are somewhat lacking, particularly in wild animal populations. Here, to examine patterns of host specificity and carbohydrate metabolism capacity, we sequenced whole genomes of Bifidobacterium isolated from wild-caught small mammals from two European countries (UK and Lithuania). Members of B. castoris, B. animalis and B. pseudolongum were detected in wild mice (Apodemus sylvaticus, A. agrarius and A. flavicollis), but not voles or shrews. B. castoris constituted the most commonly recovered Bifidobacterium (78% of all isolates), with the majority of strains only detected in a single population, although populations frequently harboured multiple co-circulating strains. Phylogenetic analysis revealed that the mouse-associated B. castoris clades were not specific to a particular location or host species, and their distribution across the host phylogeny was consistent with regular host shifts rather than host-microbe codiversification. Functional analysis suggested that mouse-derived B. castoris strains encoded an extensive arsenal of carbohydrate-active enzymes, including putative novel glycosyl hydrolases such as chitosanases that may act on chitin-derived substrates such as mushrooms or insects, along with genes encoding putative exopolysaccharides, some of which may have been acquired via horizontal gene transfer. Overall, these results provide a rare genome-level analysis of host specificity and genomic capacity among important gut symbionts of wild animals, and reveal that Bifidobacterium has a labile relationship with its host over evolutionary time scale.

microbiology↗