Xi et al., Sci. Adv.8, eabn3368 (2022) 4 May 2022SCIENCE ADVANCES | RESEARCH ARTICLE1 of 10ECOLOGYDrought soil legacy alters drivers of plant diversity-productivity relationships in oldfield systemsNianxun Xi1†‡, Dongxia Chen1†, Michael Bahn2, Hangyu Wu1, Chengjin Chu1*, Marc W. Cadotte3, Juliette M. G. Bloor4Ecosystem functions are threatened by both recurrent droughts and declines in biodiversity at a global scale, but the drought dependency of diversity-productivity relationships remains poorly understood. Here, we use a two-phase mesocosm experiment with simulated drought and model oldfield communities (360 experimental mesocosms/plant communities) to examine drought-induced changes in soil microbial communities along a plant species richness gradient and to assess interactions between past drought (soil legacies) and subsequent drought on plant diversity-productivity relationships. We show that (i) drought decreases bacterial and fungal richness and modifies relationships between plant species richness and microbial groups; (ii) drought soil legacy increases net biodiversity effects, but responses of net biodiversity effects to plant species richness are unaffected; and (iii) linkages between plant species richness and complementarity/selection effects vary depending on past and subsequent drought. These results provide mechanistic insight into biodiversity-productivity relationships in a changing environment, with implications for the stability of ecosystem function under climate change.INTRODUCTIONPlant diversity and climate change are key drivers of primary pro-ductivity and nutrient cycling (1–3). Interactions between plant diver-sity loss and the droughts associated with climate change have faced increasing attention in recent years, and widespread evidence suggests that declines in ecosystem productivity due to diversity loss may be exacerbated by drought events (4–6). Improved understanding of the mechanisms underlying the linkages between diversity- productivity relationships and drought stress is critical for climate mitigation efforts and the implementation of effective nature-based climate solutions (5, 7).Over the last 20 years, a large body of literature has emphasized the role of plant resource strategies and plant-plant interactions for plant diversity-productivity relationships (8–10). However, recent work suggests that plant-soil interactions may be equally important for plant community dynamics and biodiversity effects (BEs) (11–14). Plants can influence soil microbial community composition and generate soil legacies through the production of biochemically diverse litter and root exudates (15–17). In return, soil microbes, and fungi in particular, have the potential to modulate plant diversity- productivity relationships by enhancing complementarity effects (CEs; i.e., generating higher relative performance of species in mix-tures compared with that expected based on monocultures), because of the dilution of pathogenic effects and the accumulation of diverse soil mutualists in multispecies mixtures (12, 13, 18–23). Soil microbes may also influence plant diversity-productivity relationships via selection effects (SEs), when particular microbial groups reduce the performance of their host plant species in mixtures, thus enhancing the competitive advantage of other plant species (20, 24, 25).Environmental conditions affect soil microorganisms (26, 27), and it is therefore likely that mediation of plant diversity-productivity relationships by soil microbes may depend on local abiotic condi-tions. Many studies have documented shifts in both fungal and bacterial community composition in response to decreases in water availability and subsequent rewetting events (28–32). At the same time, drought-induced changes in plant physiology and/or plant community structure may contribute to drought soil legacies via indirect drought effects on the microbial community (33–35). Such drought soil legacies may affect longer-term plant community structure and function through plant-soil feedbacks (36–38), but the magnitude and persistence of drought legacies in soil microbes are currently subject to debate (39). To date, information on the influence of drought soil legacies on plant diversity-productivity relationships is lacking, and responses of plant diversity-productivity relationships to subsequent drought events are unclear.Here, we conducted a two-phase experiment to investigate whether and how chronic reductions in rainfall (press droughts) modify soil legacies and plant diversity-productivity relationships under subse-quent drought, with a particular focus on the role of fungal mutualists [arbuscular mycorrhizal fungi (AMF)] and pathogens. In phase I, 120 model plant communities with five species richness levels were grown in homogeneous soils under either ambient or drought con-ditions to generate “conditioned” soil samples. In phase II, newly established plant communities were provided with soil inoculums with or without previous drought exposure and subjected to either drought or ambient watering conditions (Fig. 1). Specifically, we hypothesized that (i) drought and plant species richness coinfluence soil microbial communities, (ii) drought soil legacy influences BEs on plant productivity, and (iii) subsequent drought alters effects of drought soil legacy on diversity-productivity relationships.RESULTSInteractive effects of drought and plant species richness on soil microbial communities in phase IAnalysis of soil samples across the biodiversity experiment yielded on average 594 fungal operational taxonomic units (OTUs) and 1State Key Laboratory of Biocontrol, School of Life Sciences/School of Ecology, Sun Yat-sen University, Guangzhou 510275, China. 2Department of Ecology, University of Innsbruck, 6020 Innsbruck, Austria. 3Department of Biological Sciences, University of Toronto-Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada. 4Uni-versité Clermont Auvergne, INRAE, VetAgro-Sup, UREP, 5 Chemin de Beaulieu, F-63100 Clermont-Ferrand, France.*Corresponding author. Email: chuchjin@mail.sysu.edu.cn†These authors contributed equally to this work.‡Present address: College of Forestry, Hainan University, Haikou 570228, China.Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).
Xi et al., Sci. Adv.8, eabn3368 (2022) 4 May 2022SCIENCE ADVANCES | RESEARCH ARTICLE2 of 104683 bacterial OTUs per mesocosm (fig. S1). Overall, 105 classes of bacteria and 45 classes of fungi were identified (supplementary data S1); soil fungal communities were strongly dominated by Sordariomycetes, which accounted for 51% of the sequences, whereas bacterial communities were dominated by Acidobacteriia, Alphaproteobacteria, Gammaproteobacteria, Verrucomicrobiae, and Deltaproteobacteria, which jointly represented 54% of the sequences. Fungal community structure was significantly influenced by both the level of soil moisture content (F1 = 12.94, P < 0.001) and plant species richness (F1 = 3.78, P < 0.001; Fig. 2A). These factors explained 15.13% of the variation in soil fungal community compo-sition. Bacterial community structure was also affected by the level of soil moisture content and plant species richness (soil moisture: F1 = 23.91, P < 0.001; plant species richness: F1 = 4.06, P < 0.001; Fig. 2B), together explaining 23.09% of the variation in bacterial community composition.In general, soil fungal richness decreased in response to experi-mental drought but was unaffected by plant species richness (Table 1 and Fig. 2C). In contrast, effects of plant species richness on bacterial richness differed between the ambient and drought treatments (species richness × drought interaction; Table 1 and Fig. 2D). Under ambient conditions, bacterial richness showed a negative relationship with plant species richness (adjusted R2 = 0.15 and P = 0.003), but bacterial richness was unrelated to plant species richness under drought conditions (P = 0.245; Fig. 2D). Under ambient conditions, soil moisture content also decreased with in-creasing plant species richness (fig. S2), but accounting for relation-ships between bacterial/fungal richness and soil moisture did not alter the observed relationships between bacterial/fungal richness and plant species richness (Table 1).Experimental drought also decreased AMF richness, with greatest drought-induced decreases in AMF observed under higher species richness levels (species richness × drought interaction; Table 1 and Fig. 2E). Nevertheless, AMF richness showed a positive relationship with plant species richness in both “drought” treatments (Fig. 2E; adjusted R2 = 0.29, P < 0.001 and adjusted R2 = 0.14, P = 0.003 for ambient and drought treatments respectively; table S1). Effects of plant species richness on fungal pathogen richness differed between the ambient and drought treatments (species richness × drought interaction; Table 1 and Fig. 2F). Under ambient conditions, fungal pathogen richness showed a negative relationship with plant species richness (adjusted R2 = 0.12, P = 0.007), but fungal pathogen rich-ness was unrelated to plant species richness under drought condi-tions (P = 0.145; table S1 and Fig. 2F). Fungal saprotroph richness did not show any responses to plant species richness, drought treat-ments, or their interaction (table S2 and fig. S2). In parallel, plant productivity showed a positive relationship with plant species richness under ambient conditions in phase I (adjusted R2 = 0.12, P = 0.006), but no relationship with plant species richness under drought conditions (adjusted P = 0.907; fig. S3).Plant biomass and BEs in phase IIIn general, plant aboveground biomass increased with plant species richness (Table 2, table S3, and Fig. 3A). However, the positive effects of plant species richness on aboveground biomass were greater in communities with drought soil legacy treatments (i.e., with soil previously exposed to drought) compared with those without drought soil legacy (plant species richness × drought legacy interac-tion; Table 2 and Fig. 3A). In addition, plant species richness effects were lower in mesocosms experiencing phase II drought compared with those in ambient treatments (plant species richness × phase II drought interaction; Fig. 3A).Net BEs and CEs increased with plant species richness across all drought treatments (Table 2, table S3, and Fig. 3, B and C). Positive effects of species richness were greater for ambient plant communities compared with droughted-plant communities (species Fig. 1. Schematic depiction of the experimental design. The study combined a soil legacy experiment and a plant diversity-productivity relationship experiment. In phase I, plant communities with a range of species-richness levels were grown in homogeneous soils under drought or ambient conditions to generate soil microbial legacies. In phase II, the effects of soil microbial legacies were tested on newly established plant communities grown under drought or ambient conditions, using soil inoculums conditioned by the same plant communities.
