Recovery and Community Succession of theZostera marinaRhizobiome after Transplantation

Abstract

Seagrasses can form mutualisms with their microbiomes that facilitate the exchange of energy sources, nutrients, and hormones, and ultimately impact plant stress resistance. Little is known about community succession within the belowground seagrass microbiome after disturbance and its potential role in the plant’s recovery after transplantation. We transplanted Zostera marina shoots with and without an intact rhizosphere, and cultivated plants for four weeks while characterizing microbiome recovery and effects on plant traits. Rhizosphere and root microbiomes were compositionally distinct, likely representing discrete microbial niches. Furthermore, microbiomes of washed transplants were initially different from those of sod transplants, and recovered to resemble an undisturbed state within fourteen days. Conspicuously, changes in microbial communities of washed transplants corresponded with changes in rhizosphere sediment mass and root biomass, highlighting the strength and responsive nature of the relationship between plants, their microbiome, and the environment. Potential mutualistic microbes that were enriched over time include those that function in the cycling and turnover of sulfur, nitrogen, and plant-derived carbon in the rhizosphere environment. These findings highlight the importance and resiliency of the seagrass microbiome after disturbance. Consideration of the microbiome will have meaningful implications on habitat restoration practices. Importance Seagrasses are important coastal species that are declining globally, and transplantation can be used to combat these declines. However, the bacterial communities associated with seagrass rhizospheres and roots (the microbiome) are often disturbed or removed completely prior to transplantation. The seagrass microbiome benefits seagrasses through metabolite, nutrient, and phytohormone exchange, and contributes to the ecosystem services of seagrass meadows by cycling sulfur, nitrogen, and carbon. This experiment aimed to characterize the importance and resilience of the seagrass belowground microbiome by transplanting Zostera marina with and without intact rhizospheres and tracking microbiome and plant morphological recovery over four weeks. We found the seagrass microbiome to be resilient to transplantation disturbance, recovering after fourteen days. Additionally, microbiome recovery was linked with seagrass morphology, coinciding with increases in rhizosphere sediment mass and root biomass. Results of this study can be used to include microbiome responses in informing future restoration work.

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

“…Methanol is potentially exuded by seagrass as a waste product of metabolism (Crump et al, 2018; Nemecek‐Marshall et al, 1995). Methylophilaceae and Methylophagaceae utilize methanol as a source of carbon and energy (Doronina et al, 2014) and can also be found on seagrass roots and rhizomes at lower abundances (Crump et al, 2018; Martin et al, 2020; Wang et al, 2020). Methylotrophs can produce plant growth promoting hormones and may contribute to stress tolerance in terrestrial plants (Kumar et al, 2019); they may play similar functional roles in seagrass and marine plants.…”

“…While the mechanisms for community stability are uncertain, some host species can maintain their original microbiota after transplanting, while other species exhibit microbiota turnover (Ziegler et al, 2019). Other seagrass transplant experiments investigating belowground microbiota found that seagrass transplanted without its original rhizome microbiota (rhizomes were rinsed with seawater prior to transplanting) can recover its original microbiota within 14 days (Wang et al, 2020), suggesting that host characteristics determine the microbiota.…”

The microbiota of intertidal macroalgae Fucus distichus is site‐specific and resistant to change following transplant

“…Biofilm dynamics may be a particularly important determinant of the timescale of turnover in host-associated microbial communities. Rapid microbiota turnover, on the order of hours to days, has been demonstrated for highly disturbed or previously uncolonized host surfaces and substrates in marine systems including corals (Ziegler et al, 2017(Ziegler et al, , 2019, macroalgae (Rao et al, 2006;Longford et al, 2019), seagrass (Wang et al, 2021), artificial macroalgal substrates (Lemay et al, 2020;Weigel and Pfister, 2020) and marine particles (Datta et al, 2016). Long-term observations of transplanted marine hosts with mature and unmanipulated biofilms see more gradual microbiota turnover, if any.…”

Spatial and Structural Factors Shape Seagrass-Associated Bacterial Communities in Singapore and Peninsular Malaysia

“…Considering the microbial constituents in seagrass restoration is likely even more important when using transplants from other regions, or transplants grown in ex situ nurseries, especially, as we show that microbial communities can differ over comparatively small spatial scales (<10 km). If microbes are not considered it is possible that transplants could be maladapted to their new environments, or suffer from transplantation shock (Wang et al, 2021) which could be a contributing factors leading to restoration failure (Vogel et al, 2021).…”