Seagrass (Zostera marina) transplant experiment reveals core microbiota and resistance to environmental change

Abstract

Zostera marina (seagrass) is a coastal marine angiosperm that sustains a diverse and productive ecosystem. Seagrass‐associated microbiota support host health, yet the ecological processes that maintain biodiversity and stability of the seagrass leaf microbiota are poorly understood. We tested two hypotheses: (1) Microbes select seagrass leaves as habitat such that they consistently host distinct microbiota and/or core taxa in comparison to nearby substrates, and (2) seagrass leaf microbiota are stable once established and are resistant to change when transplanted to a novel environment. We reciprocally transplanted replicate seagrass shoots (natural and surface sterilized/dead tissue treatments) among four meadows with different environmental conditions and deployed artificial seagrass treatments in all four meadows. At the end of the 5‐day experiment, the established microbiota on natural seagrass partially turned over to resemble microbial communities in the novel meadow, and all experimental treatments hosted distinct surface microbiota. We consistently found that natural and sterilized/dead seagrass hosted more methanol‐utilizing bacteria compared to artificial seagrass and water, suggesting that seagrass core microbiota are shaped by taxa that metabolize seagrass exudates coupled with minor roles for host microbial defence and/or host‐directed recruitment. We found evidence that the local environment strongly influenced the seagrass leaf microbiota in natural meadows and that transplant location explained more variation than experimental treatment. Transplanting resulted in high turnover and variability of the seagrass leaf microbiota, suggesting that it is flexibly assembled in a wide array of environmental conditions which may contribute to resilience of seagrass in future climate change scenarios.

Manipulation of the seagrass‐associated microbiome reduces disease severity

“…Microbial community composition strongly differed among eelgrass with and without a native microbiome (Figure 4, Table S5). In 2018, the 15 most abundant bacteria present at the final time point mostly belonged to Flavobacteriales and opportunistic Alteromonadales (Figure S4A; Adamczyk et al, 2022). In 2020, some bacterial taxa previously identified as key constituents of the eelgrass microbiome in other studies (Adamczyk et al, 2022; Beatty et al, 2022; Sanders‐Smith et al, 2020; Trevathan‐Tackett et al, 2020)—Flavobacteriaceae and Methylotenera —and Glaciecola were abundant on untreated eelgrass but disappeared in many bleached eelgrass samples (Figure S4B).…”

“…While eelgrass microbial communities likely differ between plants from field and lab conditions, we noted similarities in major bacterial constituents. For example, the most abundant eelgrass bacteria from the experiments and field were shared taxa, including Altermonadales ( Glaciecola ), which is easily culturable; Rhodobacteriales ( Loktanella and Sulfitobacter ), which are characteristic of the eelgrass microbiome (Adamczyk et al, 2022; Beatty et al, 2022; Crump et al, 2018; Ettinger et al, 2017; Sanders‐Smith et al, 2020); and the generalist Flavobacteriales ( Flavobacteriacea ), which is common on marine surfaces (Sanders‐Smith et al, 2020).…”

“…For example, the composition of the eelgrass leaf microbiome is variable at the meadow scale and may be due to disease prevalence, temperature, and geography (Beatty et al, 2022). Other studies find variation in the eelgrass microbiome associated with geography (Adamczyk et al, 2022;Bengtsson et al, 2017;Sanders-Smith et al, 2020) and epiphytic algae (O'Connor et al, 2022).…”

“…A growing number of studies have characterized the eelgrass microbiome (Adamczyk et al, 2022; Ettinger et al, 2017; Ettinger & Eisen, 2020; Sanders‐Smith et al, 2020; Segovia et al, 2021; Ugarelli et al, 2017). We use the term ‘microbiome’ to refer to phyllosphere bacteria and archaea living on the surface of eelgrass leaves, though we acknowledge this excludes many members of the eelgrass microbiome, including eukaryotes and viruses, as well as communities in the endosphere and rhizosphere (reviewed in Tarquinio et al, 2019).…”

“…We use the term ‘microbiome’ to refer to phyllosphere bacteria and archaea living on the surface of eelgrass leaves, though we acknowledge this excludes many members of the eelgrass microbiome, including eukaryotes and viruses, as well as communities in the endosphere and rhizosphere (reviewed in Tarquinio et al, 2019). Eelgrass leaves are selective surfaces (Kurilenko et al, 2007) with bacterial communities that are distinct from surrounding environments (Adamczyk et al, 2022; Sanders‐Smith et al, 2020). These studies provide a foundation for examining the ecological roles of the eelgrass microbiome.…”