Salinity legacy: Foliar microbiome's history affects mutualist‐conferred salinity tolerance

Abstract

The rapid human‐driven changes in the environment during the Anthropocene have placed extreme stress on many plants and animals. Beneficial interactions with microorganisms may be crucial for ameliorating these stressors and facilitating the ecosystem services host organisms provide. Foliar endophytes, microorganisms that reside within leaves, are found in essentially all plants and can provide important benefits (e.g., enhanced drought tolerance or resistance to herbivory). However, it remains unclear how important the legacy effects of the abiotic stressors that select on these microbiomes are for affecting the degree of stress amelioration provided to their hosts. To elucidate foliar endophytes' role in host‐plant salt tolerance, especially if salinity experienced in the field selects for endophytes that are better suited to improve the salt tolerance of their hosts, we combined field collections of 90 endophyte communities from 30 sites across the coastal Everglades with a manipulative growth experiment assessing endophyte inoculation effects on host‐plant performance. Specifically, we grew >350 red mangrove (Rhizophora mangle) seedlings in a factorial design that manipulated the salinity environment the seedlings experienced (freshwater vs. saltwater), the introduction of field‐collected endophytes (live vs. sterilized inoculum), and the legacy of salinity stress experienced by these introduced endophytes, ranging from no salt stress (0 parts per thousand [ppt] salinity) to high salt stress (40 ppt) environments. We found that inoculation with field‐collected endophytes significantly increased mangrove performance across almost all metrics examined (15%–20% increase on average), and these beneficial effects typically occurred when the endophytes were grown in saltwater. Importantly, our study revealed the novel result that endophyte‐conferred salinity tolerance depended on microbiome salinity legacy in a key coastal foundation species. Salt‐stressed mangroves inoculated with endophyte microbiomes from high‐salinity environments performed, on average, as well as plants grown in low‐stress freshwater, while endophytes from freshwater environments did not relieve host salinity stress. Given the increasing salinity stress imposed by sea level rise and the importance of foundation species like mangroves for ecosystem services, our results indicate that consideration of endophytic associations and their salinity legacy may be critical for the successful restoration and management of coastal habitats.

The identification of the new species Nitratireductor thuwali sp. nov. reveals the untapped diversity of hydrocarbon-degrading culturable bacteria from the arid mangrove sediments of the Red Sea

“…The two core subunits (CydA and CydB) of cytochrome bd oxidase but not the associated subunits are encoded on the genome. If the high-affinity cytochrome bd oxidase is functional in the isolate, it would not only facilitate the survival of this strain under oxygen-poor conditions (microaerophilic) typical of mangrove water-logged sediments ( Sarker et al, 2021 ), but would also confer enhanced tolerance to nitrosative stress (NO and O 2 – ), resistance to hydrogen peroxide, suppression of extracellular superoxide production and the ability to defend against antibacterial agents ( Subedi et al, 2022 ).…”

Plant species within Streptanthoid Complex associate with distinct microbial communities that shift to be more similar under drought

“…There is a positive correlation between biodiversity and ecosystem functioning; therefore, understanding how stress impacts the alpha diversity of plant‐associated bacteria can provide some information about how ecosystem functions can be affected (Jochum et al., 2020 ). A legacy effect is a phenomenon by which microbial communities that are pre‐exposed to a stress and better able to withstand subsequent stresses of the same nature (Subedi et al., 2022 ). We predicted that plants and microbes associated with serpentine soils would not be as impacted by water stress as those with an affinity to nonserpentine soils since serpentine soils can have low water‐holding capacity.…”

Phyllosphere fungal diversity generates pervasive non-additive effects on plant performance

“…Eight days after germination, seeds were aseptically planted in pots of sterile soil (262ml Heavyweight Deepots, Stuewe and Sons, Corvallis, Oregon) in the greenhouse at the University of Miami campus. Three weeks post-germination, leaves were abraded with sterilized sand and inoculated (Subedi et al, 2022) with either a single fungus from our culture collection ( i.e., monocultures), a ‘low’ microbial diversity treatment ( i.e., simple synthetic communities of 3 fungal taxa), a ‘high’ diversity treatment ( i.e., relatively more complex synthetic communities of 10 fungal taxa), or a sham inoculum of sterile water ( i.e. control treatment with no microbial addition).…”

“…a low diversity inoculum combined 5 ml of each of three randomly chosen monoculture inocula). We also treated 16 plants with a leaf slurry inoculum made by aseptically homogenizing field-collected leaves containing the natural microbiome of I. hederifolia following Subedi et al, (2022) to ensure that the effects of synthetic fungal communities in our experiment were comparable to the microbial effects experienced by plants with natural foliar microbiome communities. Plants inoculated with synthetic communities performed similarly to plants inoculated with the natural microbiome via this slurry method with 91% of synthetic communities root mass and 81% shoot mass falling within one standard deviation of performance of leaf slurry (whole microbiome-treatment) plants.…”