Experimental evidence root‐associated microbes mediate seagrass response to environmental stress

Abstract

1. Below-ground microbiota play an important role in mediating environmental conditions with important consequences for plant performance. Micro-organisms involved in plant-soil interactions may be associated with roots or bulk soil; however, the relative influence of these below-ground microbial assemblages on plant performance is poorly known, particularly for marine plants.2. We separately manipulated the root and sediment microbial assemblages of the seagrass Zostera muelleri in a fully factorial experiment to determine how these assemblages determined plant response (e.g. growth) to nutrient enrichment, a major stressor in marine systems.3. Under ambient nutrient conditions, seagrass growth was maintained regardless of root microbial assemblage disruption. Under high nutrient stress, however, seagrasses with disrupted root microbiota had reduced growth, whereas growth was maintained in seagrasses with an intact root microbiota. Disruption of bulksediment microbiota did not affect seagrass growth. Nutrient elevation was correlated with enhanced abundances of several putatively beneficial microbial taxa (e.g. sulphide-oxidising Beggiatoaceae and denitrifying Geofilum rubicundum) associated with roots. 4. Synthesis. Our results suggest that under ambient nutrient conditions microorganisms play a reduced role in influencing plant performance, but under more stressful conditions positive plant-root micro-organism interactions strengthened. These results are among the first to experimentally determine that interactions between marine plants and the root-associated microbiota are key drivers of seagrass performance under human-induced environmental changes. This suggests that as in terrestrial systems, marine plant resilience depends on the stress-mitigating functions of their root-associated microbiota and disturbance to those plant-microbiota interactions can be deleterious for plant performance.Improving our understanding of these plant-micro-organism interactions may be critical for understanding the functioning and resilience of threatened marine plants and developing more effective restoration strategies for them.

The soil microbiome affects patterns of local adaptation in an alpine plant under moisture stress

“…For example, environmental stress can determine the proportion of pathogens and mutualists, with fewer pathogens tending to be present under higher abiotic stress (Lau and Lennon, 2012;Hernandez et al, 2021). In addition, previous work has found greater benefits to fitness in plants associating with microbes under greater nutrient limitation (Johnson, 1993;Hacquard et al, 2016;David et al, 2020;Fuggle et al, 2023), less water availability (Petipas et al, 2020;Basyal and Emery, 2021), higher salinity (Lumibao et al, 2022), and greater biotic stress (Bastías et al, 2022). Dry meadow populations may have exhibited strong local adaptation because selection strength is higher in more stressful (dry) environments (Parsons, 2005;Agrawal and Whitlock, 2010).…”

Above and below-ground bacterial communities shift in seagrass beds with warmer temperatures

“…For example, prolonged marine heatwaves up to 3°C above ambient have caused seagrass mortality in temperate and subtropical regions Thomson et al, 2015;Serrano et al, 2021;Jung et al, 2023). While responses of some seagrasses to temperature changes have been well studied, the response of microbes and the role they play in ameliorating these environmental stressors has rarely been investigated (Garcias-Bonet et al, 2016;Fuggle et al, 2023).…”

“…Microbes can also influence growth, health, and productivity of seagrasses, and thus underpin ecosystem services such as nursery habitat, carbon sequestration, and coastal protection provided by seagrasses (Ugarelli et al, 2017;Brodersen et al, 2018). Microbes can have negative effects on plant performance through parasitism, resource competition, and pathogenesis, however, many microbes in the same physical niche can benefit host plant performance through nutrient acquisition and hormone production (Hansen et al, 2000;Mendes et al, 2013;Tarquinio et al, 2019;Tarquinio et al, 2019;Fuggle et al, 2023).…”

Using transplantation to restore seagrass meadows in a protected South African lagoon

“…The importance of local biotic processes, such as interspecific-interactions or the microbiome, for seagrass restoration is gaining traction ( Byers et al, 2006 ; van der Heide et al, 2011 ; Ugarelli et al, 2017 ; Fuggle, Gribben & Marzinelli, 2023 ). For example, optimising planting density can promote positive feedbacks resulting from below- and above-ground self-structuring mechanisms ( Bos & van Katwijk, 2007 ; Valdez et al, 2020 ).…”

“…Seagrasses are typically transplanted as vegetated sediment-intact cores or bare-rooted shoots (with or without anchoring) from healthy donor meadows to a restoration site ( Ganassin & Gibbs, 2008 ; Paulo et al, 2019 ; Curiel et al, 2021 ; Lange et al, 2022 ). Transplanting cores is generally recommended as the root and rhizome system remain relatively intact ( Phillips, 1990 ; Fonseca, Kenworthy & Thayer, 1998 ) and are translocated with the engineered microbiome ( Fuggle, Gribben & Marzinelli, 2023 ). Transplanting bare-rooted shoots is likely to have a lower impact on donor meadows and by selecting the appropriate anchoring material can also promote growth and prevent uprooting by wave action ( van Katwijk et al, 2016 ; Lange et al, 2022 ).…”