Host identity drives the assembly of phytoplankton microbiomes across a continental-scale environmental gradient

Host-associated microbiomes often promote host health, yet the key drivers of microbiome assembly and its consequences for host fitness remain unclear. We aimed to determine the relative roles of host identity versus the environment in driving host-microbiome assembly and the consequences of this variation in assembly for host fitness, which may help predict the resilience of host-associated microbiomes and host health amidst fluctuating environmental conditions. Here, we tracked microbiome assembly in association with initially axenic phytoplankton when incubated in seawater originating from four nearshore locations along a continental-scale environmental gradient of North America. Microbiome assembly was highly deterministic. Unexpectedly, host species identity was the overwhelming driver of microbiome community assembly despite continental-scale variation in the environment. Although secondary to host identity, the environment was a significant driver of microbiome assembly for each species evaluated, which, in turn, conferred cascading effects on host fitness as shown by thermal tolerance growth assays. We also found that host-specific microbiomes had host-specific fitness effects, particularly under thermally stressful conditions. Overall, our results advance our understanding of microbiome assembly by empirically demonstrating that although variation among host microbiomes imparted by the local environment has significant implications for host health, the host species is the overwhelming driver of microbiome assembly regardless of wide-scale variation in the environment.