Macroalgal microbiome biogeography is shaped by environmental drivers rather than geographical distance

Abstract

Abstract Background and Aims Contrasting patterns of host and microbiome biogeography can provide insight into the drivers of microbial community assembly. Distance–decay relationships are a classic biogeographical pattern shaped by interactions between selective and non-selective processes. Joint biogeography of microbiomes and their hosts is of increasing interest owing to the potential for microbiome-facilitated adaptation. Methods In this study, we examine the coupled biogeography of the model macroalga Durvillaea and its microbiome using a combination of genotyping by sequencing (host) and 16S rRNA amplicon sequencing (microbiome). Alongside these approaches, we use environmental data to characterize the relationship between the microbiome, the host, and the environment. Key Results We show that although the host and microbiome exhibit shared biogeographical structure, these arise from different processes, with host biogeography showing classic signs of geographical distance decay, but with the microbiome showing environmental distance decay. Examination of microbial subcommunities, defined by abundance, revealed that the abundance of microbes is linked to environmental selection. As microbes become less common, the dominant ecological processes shift away from selective processes and towards neutral processes. Contrary to expectations, we found that ecological drift does not promote structuring of the microbiome. Conclusions Our results suggest that although host macroalgae exhibit a relatively ‘typical’ biogeographical pattern of declining similarity with increasing geographical distance, the microbiome is more variable and is shaped primarily by environmental conditions. Our findings suggest that the Baas Becking hypothesis of ‘everything is everywhere, the environment selects’ might be a useful hypothesis to understand the biogeography of macroalgal microbiomes. As environmental conditions change in response to anthropogenic influences, the processes structuring the microbiome of macroalgae might shift, whereas those governing the host biogeography are less likely to change. As a result, increasingly decoupled host–microbe biogeography might be observed in response to such human influences.