Having the 'right' microbiome matters for host trait expression and the strength of mutualism between duckweeds and microbes

An organisms phenotypes and fitness often depend on interactive effects of its genome (Ghost), microbiome (Gmicrobe), and environment (E). These G xG, G xE, and G xG xE effects fundamentally shape host-microbiome (co)evolution and may be widespread, but are rarely compared within a single experiment. We collected and cultured Lemna minor (duckweed) and its associated microbiome from 10 sites across an urban-to-rural ecotone. We factorially manipulated host genotype and microbiome in two environments (low and high zinc, an urban aquatic stressor) in an experiment with 200 treatments: 10 host genotypes x 10 microbiomes x 2 environments. Host genotype explained the most variation in L. minor fitness and traits, while microbiome effects depended on host genotype (G xG) or environment (G xE). Hosts had higher fitness and microbes grew fastest when tested microbiomes more closely matched field microbiomes, suggesting some local adaptation between hosts and their microbiota. High microbiome similarity also led to more predictable host trait expression. In contrast, although zinc decreased host fitness, we observed no local adaptation of urban duckweed or microbes to high-zinc conditions. Thus, we found that host fitness and trait expression are contingent on microbiome composition, with implications for microbiome engineering and host-microbiome evolution.