The macroecology of butyrate-producing bacteria via metagenomic assessment of butyrate production capacity

Joel E Brame; Craig Liddicoat; Catherine A Abbott; Robert A Edwards; Jake M Robinson; Nicolas E Gauthier; Martin F Breed

doi:10.1002/ece3.11239

The macroecology of butyrate-producing bacteria via metagenomic assessment of butyrate production capacity

Ecol Evol. 2024 Apr 29;14(5):e11239. doi: 10.1002/ece3.11239. eCollection 2024 May.

Authors

Joel E Brame¹, Craig Liddicoat^{1

2}, Catherine A Abbott¹, Robert A Edwards¹, Jake M Robinson¹, Nicolas E Gauthier³, Martin F Breed¹

Affiliations

¹ College of Science and Engineering Flinders University Bedford Park South Australia Australia.
² School of Public Health The University of Adelaide Adelaide South Australia Australia.
³ Florida Museum of Natural History University of Florida Gainesville Florida USA.

Abstract

Butyrate-producing bacteria are found in many outdoor ecosystems and host organisms, including humans, and are vital to ecosystem functionality and human health. These bacteria ferment organic matter, producing the short-chain fatty acid butyrate. However, the macroecological influences on their biogeographical distribution remain poorly resolved. Here we aimed to characterise their global distribution together with key explanatory climatic, geographical and physicochemical variables. We developed new normalised butyrate production capacity (BPC) indices derived from global metagenomic (n = 13,078) and Australia-wide soil 16S rRNA (n = 1331) data, using Geographic Information System (GIS) and modelling techniques to detail their ecological and biogeographical associations. The highest median BPC scores were found in anoxic and fermentative environments, including the human (BPC = 2.99) and non-human animal gut (BPC = 2.91), and in some plant-soil systems (BPC = 2.33). Within plant-soil systems, roots (BPC = 2.50) and rhizospheres (BPC = 2.34) had the highest median BPC scores. Among soil samples, geographical and climatic variables had the strongest overall effects on BPC scores (variable importance score range = 0.30-0.03), with human population density also making a notable contribution (variable importance score = 0.20). Higher BPC scores were in soils from seasonally productive sandy rangelands, temperate rural residential areas and sites with moderate-to-high soil iron concentrations. Abundances of butyrate-producing bacteria in outdoor soils followed complex ecological patterns influenced by geography, climate, soil chemistry and hydrological fluctuations. These new macroecological insights further our understanding of the ecological patterns of outdoor butyrate-producing bacteria, with implications for emerging microbially focused ecological and human health policies.

Keywords: butyrate; ecosystem services; gut microbiome; metagenomics; microbial ecology; soil microbiota.