Habitat filtering more than microbiota origin controls microbiome transplant outcomes in soil

Abstract Human activities cause a global loss of soil microbiome diversity and functionality. One way to reverse this trend is through microbiota transplants, but the processes determining merger outcomes are not well understood. Here, we investigated the roles of habitat filtering and microbiota origin on microbiome development upon mergers, with the hypothesis that native strains are better adapted to their own habitat and will outcompete non-native ones in niche colonization. To test this, we contrasted community development in soil microcosms between two taxa-diverse microbiota originating from either topsoil (SoilCom) or freshwater lake (LakeCom), and a defined mixture of 21 soil bacteria (SynCom). When inoculated separately, SoilCom and LakeCom showed similar taxa and colonization patterns contributing to community growth and decline within the soil microcosms. SynCom transplants to either SoilCom or LakeCom under renewed growth conditions permanently altered their community trajectories, and slightly further converged their taxa compositions. Levels of SynCom members in both resident backgrounds decreased from initial 50-80% to below 1% within two months. Merged as well as non-merged communities resembled natural soils in comparison to over 81,000 publicly available soil, sediment, and lake microbiomes. Our results show that habitat filtering is dominant over microbiota taxa origin in determining transplant outcomes. Even though the proliferation of SynCom transplants remained limited, their capacity to influence community merger trajectories long term opens new paths for soil microbiome engineering.