Contrasting effects of rhizosphere and sediment microbiota on seagrass performance in response to a simulated marine heatwave

Climate change-induced temperature stress is drastically affecting the health and survival of plants across terrestrial and aquatic ecosystems. For terrestrial plants, below-ground microbes can enhance plant performance in response to environmental stress and recent evidence suggests a similar role for marine plants. Despite this, the potential for below-ground microbes to enhance marine plant resilience against climate change-induced marine heatwaves (MHWs), an ocean temperature stress that is increasing in frequency and intensity globally, remains unclear.

We experimentally manipulated microbial communities in the Zostera muelleri rhizosphere and bulk sediment through root sterilisation and sediment autoclaving to determine their influence on seagrass growth and survival under two marine heatwave scenarios (recent MHW profile and an end-of-century scenario).

Seagrasses with an experimentally disrupted rhizosphere microbiome showed reduced growth under all temperature and sediment treatments. In contrast, an intact bulk sediment microbiome hindered plant growth under the future marine heatwave scenario and disruption of these communities had a positive effect on plant performance. Future marine heatwave treatments had a lower relative abundance of potentially beneficial microbes in bulk sediments (i.e., Akkermansiaceae) and were enriched with potential plant pathogens (i.e., Xanthomonadaceae). In addition, the rhizosphere of plants in intact bulk sediments showed a lower relative abundance of potential plant-growth promoting bacteria.

Synthesis. This study provides experimental evidence that marine heatwaves can negatively affect seagrass performance via changes in bulk sediment microbiota and that the benefits provided by rhizosphere microbiota to plants may not be enough to overcome such effects. Our experiment highlights for the first time the importance of below-ground microbes in seagrass responses to heat stress. Furthermore, our findings emphasise the need to consider microbial interactions in future seagrass research and suggest that shifts in microbial communities could play a key role in seagrass resilience to climate change. Furthermore, these insights may be crucial for restoration efforts, as integrating microbial communities into seagrass management strategies may enhance the success of restoration initiatives under changing environmental conditions.

Methods
The experiment was designed to evaluate the effects of sediment microbiota, rhizosphere microbiota and marine heatwaves on the growth and survival of the seagrass Zostera muelleri. Sediments from a seagrass meadow were collected and processed to create treatments with intact and disrupted (sterilised) microbiota. Seagrass shoots were also collected, standardised, and treated to either maintain or disrupt root-associated microbes.  Seagrass shoots were planted in the pots, which were then deployed in pots at the aquarium facilities of the Sydney Institute of Marine Sciences (SIMS) under three different temperature treatments.