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

Abstract Climate change‐induced temperature stress is affecting the performance 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 Zostera muelleri rhizosphere and bulk sediments 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 how below‐ground microbes influence seagrass responses to heat stress. Furthermore, our findings emphasise the need to consider below‐ground microbial interactions in future seagrass research and suggest that shifts in microbial communities may play a role in seagrass resilience to climate change. These insights may be critical for restoration efforts, as integrating below‐ground microbial communities into seagrass management strategies may enhance the success of restoration initiatives under changing environmental conditions.