Renske Jongen

Summary: Belowground microbes are increasingly recognised as mediators of plant responses to stress, but it remains unclear whether the thermal histories of marine plants and their associated belowground microbes influence plant performance under ocean warming. We conducted a common‐garden field experiment at a long‐term warmed site in Lake Macquarie (NSW, Australia, > 30 yr, 1–3°C warming), to test the effects of sediment origin (ambient vs warm‐origin), plant origin (ambient vs warm‐origin) and microbial disruption (intact vs disrupted rhizosphere and bulk sediment microbial communities) on seagrass ( Zostera muelleri ) performance. Both plant origins had lower aboveground biomass in intact warm‐origin sediments, but warm‐origin plants recovered when bulk sediment microbial communities were disrupted, indicating that warming‐altered sediment microbial communities can suppress seagrass performance. Disrupted warm‐origin sediments were enriched in sulphide‐oxidising bacteria, which likely contributed to enhanced performance. In warm‐origin sediments, rhizosphere bacterial communities were similar across plant origins, indicating that sediments shape rhizosphere bacterial assembly. Rhizosphere microbial disruption had no effect on plant performance. We show that ocean warming can shape sediment microbial communities in ways that suppress seagrass performance, suggesting that sediment microbial communities can override plant thermal history and act as hidden constraints on seagrass tolerance to warming.

Soil nutrient availability fluctuates widely in the environment creating stressful conditions for plants. Below‐ground microbial communities can help plants cope with nutrient stress, yet the relative importance of rhizosphere and bulk soil microbial communities across a spectrum of nutrient conditions remains unclear, particularly for marine plants. We experimentally manipulated nutrient availability and the rhizosphere and sediment (analogous to soil) microbial communities of the seagrass Zostera muelleri in pots in the field to determine the effects of below‐ground microbial communities (disrupted or intact) on seagrass performance under low‐, medium‐ and high‐nutrient treatments. Disrupting rhizosphere or bulk sediment microbial communities had no effect on above‐ground biomass. However, disrupting rhizosphere or sediment microbial communities reduced root biomass under low‐ and high‐nutrient treatments compared to medium‐nutrient treatments, suggesting that below‐ground microbial communities mediate seagrass responses to nutrient stress. Under both low‐ and high‐nutrient treatments, the bacterial community composition of the rhizosphere and bulk sediment differed when microbial communities were intact compared to when they were disrupted. Under low‐nutrient treatments, we identified a higher relative abundance of potential nutrient‐cycling taxa, that is Flavobacteria, Methyloligellaceae and Desulfocapsaceae in the rhizosphere than under other nutrient treatments. No specific taxa in the rhizosphere changed in relative abundance under high‐nutrient conditions. Synthesis . This study suggests that below‐ground microbial communities are central to how seagrasses cope with nutrient variability. By providing field‐based, experimental evidence that both rhizosphere and bulk soil communities shape root growth, our work extends ecological understanding of plant–microbe interactions beyond terrestrial systems and into the marine realm. These findings underscore the importance of below‐ground interactions for predicting marine plant resilience to environmental change and highlight the need to incorporate below‐ground microbes into conservation and restoration strategies.

Seagrass–microbe interactions are crucial for seagrass performance and the coastal ecosystem services they support. However, significant variation in experimental and analytical approaches has hindered our broader understanding of seagrass–microbe interactions and the potential existence of a functional core microbiome, i.e. microbial taxa that are consistently present on hosts and likely exert a disproportionate impact on host function. Through a systematic review, we aimed first to understand current trends and knowledge gaps in seagrass–microbe research. Additionally, we conducted a systematic mapping of global 16S ribosomal RNA (rRNA) gene sequencing data to characterise core bacterial taxa in three plant microenvironments (leaves, roots and rhizosphere) across multiple species and within a highly studied seagrass species, Zostera marina . The results revealed a growing number of studies since the 2010s manipulating environmental variables and/or seagrass microbes to investigate their roles in seagrass performance and responses to stressors. Most studies have primarily focused on seagrass leaves, examined a limited number of species, and investigated only bacteria via 16S rRNA gene amplicon sequencing. A few studies attempted to characterise seagrass core microbiomes, often using highly variable approaches to define core taxa. Our systematic mapping based on global sequencing data allowed the identification of prevalent bacterial taxa belonging to the families Desulfocapsaceae and Sulfurovaceae in the seagrass rhizosphere, which may play an important role in the performance of Z. marina and other seagrass species. The results also showed that many other bacterial families were prevalent across different seagrass microenvironments, such as Rhodobacteraceae and Flavobacteriaceae , with substantial taxonomic variability and functional metabolic redundancy. We identified key challenges stemming from available data and variable methodologies and provided insights to guide future experimental work and deepen our understanding of seagrass–microbe interactions. We argue that such knowledge may improve seagrass management outcomes, especially by informing restoration strategies based on core microbial taxa.

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.

Seagrass meadows are declining globally at alarming rates due to multiple stressors. Efforts are underway to preserve and restore these valuable ecosystems. Several frameworks for seagrass restoration exist, and some restoration attempts are being made at scale; however, poor outcomes are widespread, suggesting our understanding of the processes that drive seagrass performance is still limited. We argue that plant-sediment interactions influence almost all components of restoration, yet they are poorly incorporated in restoration design and frameworks. We synthesise the current information on how belowground interactions influence seagrass health and identify which of these are amenable to manipulation and at what scale they could be employed to improve restoration strategies and decision-making frameworks. We identified three key, interdependent areas by which belowground interactions influence seagrass health and performance. Those three areas include how (1) sediment microbial communities control nutrient and chemical cycling for seagrass, (2) the response of seagrass to sediment processes may be influenced by their life history and genetics of seagrass species targeted for restoration and (3) other species may interact with sediments to promote or inhibit seagrass survivorship and growth. Decision-making frameworks should be extended to include belowground interactions because they are of fundamental concern for determining initial site suitability and affect subsequent decisions and planning for restoration. This, in turn, will improve restoration outcomes and community engagement, critical for the successful management of these endangered ecosystems.

Purpose: Insect herbivory affects plant growth, nutrient and secondary metabolite concentrations and litter quality. Changes to litter quality due to insect herbivory can alter decomposition, with knock on effects for plant growth mediated through the plant-litter-soil feedback pathway.Methods: Using a multi-phase glasshouse experiment, we tested how changes in shoot and root litter quality of fast- and slow-growing grass caused by insect herbivores affect the performance of response plants in the soil in which the litter decomposed.Results: We found that insect herbivory resulted in marginal changes to litter quality and did not affect growth when plants were grown with fast- versus slow-growing litter. Overall, presence of litter resulted in reduced root and shoot growth and this effect was significantly more negative in shoots versus roots. However, this effect was minimal, with a loss ofc.1.4% and 3.1% dry weight biomass in roots versus shoots, respectively. Further, shoot litter exposed to insect herbivory interacted with response plant identity to affect root growth.Conclusions: Our results suggest that whether litter originates from plant tissues exposed to insect herbivory or not and its interaction with fast- versus slow-growing grasses is of little importance, but species-specific responses to herbivory-conditioned litter can occur. Taken collectively, the overall role of the plant-litter-soil feedback pathway, as well as its interaction with insect herbivory, is unlikely to affect broader ecosystem processes in this system.

Plants leave legacy effects in the soil they grow in, which can drive important vegetation processes, including productivity, community dynamics and species turnover. Plants at the same time also face continuous pressure posed by insect herbivores. Given the intimate interactions between plants and herbivores in ecosystems, plant identity and herbivory are likely to interactively shape soil legacies. However, the mechanisms that drive such legacy effects on future generations of plants and associated herbivores are little known. In a greenhouse study, we exposed 10 common grasses and non‐leguminous forbs individually to insect herbivory by two closely related noctuid caterpillars, Mamestra brassicae and Trichoplusia ni (Lepidoptera: Noctuidae) or kept them free of herbivores. We then used the soil legacies created by these plant individuals to grow a plant community composed of all 10 plant species in each soil and exposed these plant communities to M. brassicae. We measured conditioning plant biomass, soil respiration and chemistry of the conditioned soils, as well as individual plant, plant community and herbivore biomass responses. At the end of the conditioning phase, soils with herbivore legacies had higher soil respiration, but only significantly so for M. brassicae. Herbivore legacies had minimal impacts on community productivity. However, path models reveal that herbivore‐induced soil legacies affected responding herbivores through changes in plant community shoot: root ratios. Soil legacy effect patterns differed between functional groups. We found strong plant species and functional group‐specific effects on soil respiration parameters, which in turn led to plant community shifts in grass: forb biomass ratios. Soil legacies were negative for the growth of plants of the same functional group. Synthesis. We show that insect herbivory, plant species and their functional groups, all incur soil microbial responses that lead to subtle (herbivory) or strong (plants and their functional group) effects in response plant communities and associated polyphagous herbivores. Hence, even though typically ignored, our study emphasizes that legacies of previous insect herbivory in the soil can influence current soil–plant–insect community interactions. A free Plain Language Summary can be found within the Supporting Information of this article.