Diversity-function Relationships Research Articles

Diversity–functioning relationships across hierarchies of biological organization

Numerous biodiversity–ecosystem functioning (BEF) experiments have shown that plant community productivity typically increases with species diversity. In these studies, diversity is generally quantified using metrics of taxonomic, phylogenetic, or functional differences among community members. Research has also shown that the relationships between species diversity and functioning depends on the spatial scale considered, primarily because larger areas may contain different ecosystem types and span gradients in environmental conditions, which result in a turnover of the species set present locally. A fact that has received little attention, however, is that ecological systems are hierarchically structured, from genes to individuals to communities to entire landscapes, and that additional biological variation occurs at levels of organization above and below those typically considered in BEF research. Here, we present cases of diversity effects at different hierarchical levels of organization and compare these to the species‐diversity effects traditionally studied. We argue that when this evidence is combined across levels, a general framework emerges that allows the transfer of insights and concepts between traditionally disparate disciplines. Such a framework presents an important step towards a better understanding of the functional importance of diversity in complex, real‐world systems.

Community composition, and not species richness, of microbes influences decomposer functional diversity in soil

Diversity-function relationships in producers, and how these are influenced by consumers, are well known. However, these are not well known for microbial decomposers in soil. It is also unknown whether and how consumers such as large mammalian herbivores influence soil microbial decomposer diversity-function relationships. We used a 14-year-old herbivore-exclusion experiment in the Trans-Himalayan drylands of northern India to address whether microbial functions vary with microbial diversity (both species richness and composition), and whether herbivores alter the diversity-function relationships. We analyzed soils from n = 10 paired grazed-and-fenced plots three times during the growth season of 2019. Data were from 16S rDNA gene amplicon sequencing of 7.6 million reads covering 1937 operational taxonomic units (OTU) of bacteria across 47 phyla (of which 924 OTUs were identifiable to genus level), and 1800 catabolic profiles across 30 substrates related to carbon metabolism. We found that functional diversity was positively related to microbial community composition, but not to species richness; it was also unaffected by large mammalian herbivore-exclusion to indicate resilience and resistance. This positive relationship between community composition and functional diversity challenges the prevailing notion of functional redundancy in hyper-diverse soil microbial communities since certain combinations of species could outperform others and determine decomposition processes and services. Structural equation models suggested that the strength of this relationship is favoured by availability of soil moisture. Microbial functions varied more strongly with temporal variables (e.g., seasonality) than with spatial variables (e.g., edaphic factors such as soil texture and pH). Although interpretations can be constrained by which and how many functions are investigated, the relationship was generalizable and robust once 16 or more functions were quantified. Decomposition in drylands may be particularly susceptible to how the identity of the microbial species, and not the number of species, responds to rising precipitation variability under ongoing and projected climate change.

Niche complementarity among plants and animals can alter the biodiversity–ecosystem functioning relationship

Abstract Species‐rich communities exhibit higher levels of ecosystem functioning compared with species‐poor ones, and this positive relationship strengthens over time. One proposed explanation for this phenomenon is the reduction of niche overlap among plants or animals, which corresponds to increased complementarity and reduced competition. In order to examine the potential of increased complementarity among plants or animals to strengthen the relationship between diversity and ecosystem functions, we integrated models of bio‐energetic population dynamics and food‐web assembly. Through the simulation of various scenarios of plant and animal complementarity change, we sought to elucidate the mechanisms underlying the observed increases in (1) primary productivity, (2) control of herbivores by predators and (3) reduction of herbivore pressure on plants in species‐rich communities. Our findings reveal that increased niche complementarity of plants can steepen the diversity–function relationships if it does not increase their intraspecific competition, while increasing complementarity among animals during community assembly can also have a positive effect but with considerable variability. The study highlights the importance of trait variation both among and within species and the interplay between intra‐ and interspecific competition strength in shaping the functioning of ecosystems over time. These results offer insights into the mechanisms underpinning the diversity–functioning relationship and have practical implications for ecosystem management and conservation efforts. Read the free Plain Language Summary for this article on the Journal blog.

Multifunctional redundancy: Impossible or undetected?

The diversity-functioning relationship is a pillar of ecology. Two significant concepts have emerged from this relationship: redundancy, the asymptotic relationship between diversity and functioning, and multifunctionality, a monotonic relationship between diversity and multiple functions occurring simultaneously. However, multifunctional redundancy, an asymptotic relationship between diversity and multiple functions occurring simultaneously, is rarely detected in research. Here we assess whether this lack of detection is due to its true rarity, or due to systematic research error. We discuss how inconsistencies in the use of terms such as 'function' lead to mismatched research. We consider the different techniques used to calculate multifunctionality and point out a rarely considered issue: how determining a function's maximum rate affects multifunctionality metrics. Lastly, we critique how a lack of consideration of multitrophic, spatiotemporal, interactions and community assembly processes in designed experiments significantly reduces the likelihood of detecting multifunctional redundancy. Multifunctionality research up to this stage has made significant contributions to our understanding of the diversity-functioning relationship, and we believe that multifunctional redundancy is detectable with the use of appropriate methodologies.

Hierarchical metacommunity structure of fungal endophytes.

The ecological and evolutionary processes shaping community structure and functions of microbial symbionts are known to be scale-dependent. Nonetheless, understanding how the relative importance of these processes changes across spatial scales, and deciphering the hierarchical metacommunity structure of fungal endophytes has proven challenging. We investigated metacommunities of endophytic fungi within leaves of an invasive plant (Alternanthera philoxeroides) across wide latitudinal transects both in its native (Argentina) and introduced (China) ranges to test whether metacommunities of fungal endophytes were structured by different drivers at different spatial scales. We found Clementsian structures with seven discrete compartments (distinctive groups of fungal species with coincident distribution ranges), which coincided with the distribution of major watersheds. Metacommunity compartments were explicitly demarcated at three spatial scales, that is, the between-continent, between-compartment, and within-compartment scales. At larger spatial scales, local environmental conditions (climate, soil, and host plant traits) were replaced by other geographical factors as principal determinants of metacommunity structure of fungal endophytes and community diversity-function relationships. Our results reveal novel insights into the scale dependency of diversity and functions of fungal endophytes, which are likely similar for plant symbionts. These findings can potentially improve our understanding of the global patterns of fungal diversity.

Community context mediates effects of pollinator loss on seed production

AbstractA critical goal for ecologists is understanding how ongoing local and global species losses will affect ecosystem functions and services. Diversity–functioning relationships, which are well‐characterized in primary producer communities, are much less consistently predictable for ecosystem functions involving two or more trophic levels, particularly in situations where multiple species in one trophic level impact functional outcomes at another trophic level. This is particularly relevant to pollination functioning, given ongoing pollinator declines and the value of understanding pollination functioning for single plant species like crops or threatened plants. We used spatially replicated, controlled single‐pollinator‐species removal experiments to assess how changes in bumble bee species richness impacted the production of fertilized seeds in a perennial herb—Delphinium barbeyi—in the Rocky Mountains of Colorado, USA. To improve predictability, we also assessed how traits and abundances in the plant and bumble bee communities were related to D. barbeyi reproductive success. We hypothesized that trait‐matching between pollinator proboscis length and D. barbeyi's nectar spurs would produce a greater number of fertilized seeds, while morphological similarity within the floral community would dilute pollination services. We found that the effects of pollinator removal differed depending on the behavioral patterns of pollinators and compositional features of the plant and pollinator communities. While pollinator floral fidelity generally increased D. barbeyi seed production, that positive effect was primarily evident when more than half of the Bombus community was experimentally removed. Similarly, communities comprising primarily long‐tongued bees were most beneficial to D. barbeyi seed production in tandem with a strong removal. Finally, we observed contrasting effects of morphological similarity in the plant community, with evidence of both competition and facilitation among plants. These results offer an example of the complex dynamics underlying ecosystem function in multitrophic systems and demonstrate that community context can impact diversity–functioning relationships between trophic levels.

Effects of nitrogen deposition on carbon and nutrient cycling along a natural soil acidity gradient as revealed by metagenomics.

Nitrogen (N) deposition and soil acidification are environmental challenges affecting ecosystem functioning, health, and biodiversity, but their effects on functional genes are poorly understood. Here, we utilized metabarcoding and metagenomics to investigate the responses of soil functional genes to N deposition along a natural soil pH gradient. Soil N content was uncorrelated with pH, enabling us to investigate their effects separately. Soil acidity strongly and negatively affected the relative abundances of most cluster of orthologous gene (COG) categories of the metabolism supercategory. Similarly, soil acidity negatively affected the diversity of functional genes related to carbon and N but not phosphorus cycling. Multivariate analyses showed that soil pH was the most important factor affecting microbial and functional gene composition, while the effects of N deposition were less important. Relative abundance of KEGG functional modules related to different parts of the studied cycles showed variable responses to soil acidity and N deposition. Furthermore, our results suggested that the diversity-function relationship reported for other organisms also applies to soil microbiomes. Since N deposition and soil pH affected microbial taxonomic and functional composition to a different extent, we conclude that N deposition effects might be primarily mediated through soil acidification in forest ecosystems.

Canopy structure: An intermediate factor regulating grassland diversity-function relationships under human disturbances.

Grasslands are one of the largest coupled human-nature terrestrial ecosystems on Earth, and severe anthropogenic-induced grassland ecosystem function declines have been reported recently. Understanding factors influencing grassland ecosystem functions is critical for making sustainable management policies. Canopy structure is an important factor influencing plant growth through mediating within-canopy microclimate (e.g., light, water, and wind), and it is found coordinating tightly with plant species diversity to influence forest ecosystem functions. However, the role of canopy structure in regulating grassland ecosystem functions along with plant species diversity has been rarely investigated. Here, we investigated this problem by collecting field data from 170 field plots distributed along an over 2000km transect across the northern agro-pastoral ecotone of China. Aboveground net primary productivity (ANPP) and resilience, two indicators of grassland ecosystem functions, were measured from field data and satellite remote sensing data. Terrestrial laser scanning data were collected to measure canopy structure (represented by mean height and canopy cover). Our results showed that plant species diversity was positively correlated to canopy structural traits, and negatively correlated to human activity intensity. Canopy structure was a significant indicator for ANPP and resilience, but their correlations were inconsistent under different human activity intensity levels. Compared to plant species diversity, canopy structural traits were better indicators for grassland ecosystem functions, especially for ANPP. Through structure equation modeling analyses, we found that plant species diversity did not have a direct influence on ANPP under human disturbances. Instead, it had a strong indirect effect on ANPP by altering canopy structural traits. As to resilience, plant species diversity had both a direct positive contribution and an indirect contribution through mediating canopy cover. This study highlights that canopy structure is an important intermediate factor regulating grassland diversity-function relationships under human disturbances, which should be included in future grassland monitoring and management.

Variation in diversity-function relationships can be explained by species interactions.

Research Highlight: Wu, D., Xu, C., Wang, S., Zhang, L., & Kortsch, S. (2022). Why are biodiversity-ecosystem functioning relationships so elusive? Trophic interactions may amplify ecosystem function variability. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13808. There is consensus that average trends of ecosystem functions increase with species diversity. However, large variations in ecosystem function (VEF) in systems with similar diversity levels are commonly observed, yet not understood. In this study, Wu et al. (2022) integrate empirical aquatic food webs with a multitrophic model to show that VEF generally shows a hump-shaped pattern along the species richness gradient. This pattern is related to changes in taxa composition across trophic levels-the proportion of consumer species relative to basal species-along the gradient of species richness. Thus, VEF dependence on species diversity is driven by both bottom-up and top-down control that regulate taxa composition and taxa dominance. These results are corroborated with an independent food web dataset from the Gulf of Riga. An important implication of this study is that biodiversity loss may not only reduce the mean levels of ecosystem functioning, but also increase unpredictability of functions by generating greater function variability.

Loss of microbial diversity weakens specific soil functions, but increases soil ecosystem stability

The importance of microbial community diversity for soil functioning is still debated. Here, we used a dilution approach (undiluted, and 10−4, 10−8 and 10−12) and supplementation of N nutrient and electron donors to reveal the response of specialized soil functions (lindane removal, methanogenesis and Fe(III) reduction) and microbiome stability in an eutrophic environment. Contrasting to our previous findings in oligotrophic condition, the loss of diversity delayed lindane degradation (with residual concentration of 11.88 mg kg−1 on an average in diluted vs 1.23 mg kg−1 in undiluted), as well as significantly inhibited Fe(III) reduction and methanogenesis. Dilution under eutrophic conditions also weakened the coupling intensity between lindane degradation and methanogenesis, associating with the abundance reduction of specialized dechlorinators and methanogens. However, decline of microbial diversity significantly aggravated the microbial respiration. Microbial co-occurrence networks under diversity loss became more robust, with microbiome stability significantly correlated with abundant species and network complexity. Collectively, nutrient status determined the interaction strength among functional bacterial and archaeal groups, thereby driving contrast in the dependence of specialized and generalist soil functioning on microbial diversity. These findings provide new insights into improved evaluation of carbon loss and extended diversity-functioning relationships to a multi-factor context.

Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems.

ABSTRACTTraditional fermentation processes are driven by complex fungal microbiomes. However, the exact means by which fungal diversity affects fermentation remains unclear. In this study, we systematically investigated the diversity of a fungal community and its functions during the multibatch Baijiu fermentation process. Metabolomics analysis showed that the metabolic profiles of the Baijiu were enhanced with an increase in the fermentation time, as determined from the characteristic volatile flavors. High-throughput sequencing technology revealed that the major fungal species involved in sauce-flavor Baijiu fermentation are Pichia sp. (41.75%, average relative abundance), Saccharomyces sp. (13.07%), thermophilic species (9.16%), Monascus sp. (6.80%), Aspergillus sp. (4.69%), Schizosaccharomyces sp. (3.76%), Thermomyces sp. (3.74%), and Zygosaccharomyces sp. (1.41%). In addition, the fungal diversity increased as the number of fermentation batches increased. Moreover, the increased fungal diversity contributed to the modularity of the fungal communities, wherein Pichia sp., Torulaspora sp., and Saccharomyces sp. maintained the stability of the fungal community. In addition, metatranscriptomics sequencing technologies were used to reconstruct the key metabolic pathways during fermentation, and it was found that the increased microbial diversity significantly promoted glucose-mediated carbon metabolism. Finally, functional gene analysis showed that functional microorganisms, such as Zygosaccharomyces and Pichia, can enhance fermentation as a result of the high expression of pyruvate decarboxylase and propanol-preferring alcohol dehydrogenase during the metabolism of pyruvate. These results indicate that fungal biodiversity can be exploited to enhance fermentation-based processes via network interactions and metabolism during multiple-batch fermentation.IMPORTANCE Biodiversity and network interactions act simultaneously on the microbial community structure in the Baijiu fermentation process, thereby rendering the microbiome dynamics challenging to manage and predict. Understanding the complex fermentation community and its relationship to community functions is therefore important in the context of developing improved fermentation biotechnology systems. Our work demonstrates that multiple-batch fermentation steps increase microbial diversity and promote community stability. Crucially, the enhanced modularity in the microbial network increases the metabolism of flavor compounds and ethanol. This study highlights the power of biodiversity and network interactions in regulating the function of the microbiome in food fermentation ecosystems.

Microbiome assembly predictably shapes diversity across a range of disturbance frequencies in experimental microcosms

Diversity is often implied to have a positive effect on the functional stability of ecological communities. However, its relationship with stochastic and deterministic assembly mechanisms remains largely unknown, particularly under fluctuating disturbances. Here, we subjected complex bacterial communities in microcosms to different frequencies of alteration in substrate feeding scheme, tracking temporal dynamics in their assembly, structure and function. Activated sludge bioreactors were subjected to six different frequencies of double organic loading, either never (undisturbed), every 8, 6, 4, or 2 days (intermediately disturbed), or every day (press disturbed), and operated in daily cycles for 42 days. Null modeling revealed a stronger role of stochastic assembly at intermediate disturbance frequencies, with a peak in stochasticity that preceded the occurrence of a peak in α-diversity. Communities at extreme ends of the disturbance range had the lowest α-diversity and highest within-treatment similarity in terms of β-diversity, with stronger deterministic assembly. Increased carbon removal and microbial aggregate settleability (general functions) correlated with stronger deterministic processes. In contrast, higher stochasticity correlated with higher nitrogen removal (a specialized function) only during initial successional stages at intermediate disturbance frequencies. We show that changes in assembly processes predictably precede changes in diversity under a gradient of disturbance frequencies, advancing our understanding of the mechanisms behind disturbance–diversity–function relationships.

Crop performance is predicted by soil microbial diversity across phylogenetic scales

AbstractSoils contain diverse living communities that provide key ecosystem functions in agroecosystems. In many systems, ecosystem functions are positively related to the taxonomic, phylogenetic, and functional diversity of the community. Despite calls to incorporate microbial diversity in measures of soil health, whether increased microbial diversity per se can predict increased crop health and productivity has rarely been documented. Here, we used microbial communities from commercial potato fields varying in diversity and composition, and experimentally assessed their ability to promote crop yield under low or high nutrient conditions and to suppress a soil‐borne pathogen. Across two independent sets of communities, we found that yields under low nutrient conditions were predicted by high initial microbial diversity measured at broad phylogenetic levels, consistent with greater niche complementarity among unrelated taxa leading to greater total resource use. However, disease suppression was inconsistently linked to diversity and was explained as well or better by microbial composition rather than diversity per se. Ecosystem multifunctionality was predicted by high diversity at broad to intermediate phylogenetic scales. These results indicate that the diversity of microbial taxa may influence multiple soil functions; however, the mechanisms underlying the diversity–function relationships may vary.

Climate-Driven Legacies in Simulated Microbial Communities Alter Litter Decomposition Rates

The mechanisms underlying diversity-functioning relationships have been a consistent area of inquiry in biogeochemistry since the 1950s. Though these mechanisms remain unresolved in soil microbiomes, many approaches at varying scales have pointed to the same notion—composition matters. Confronting the methodological challenge arising from the complexity of microbiomes, this study used the model DEMENTpy, a trait-based modeling framework, to explore trait-based drivers of microbiome-dependent litter decomposition. We parameterized DEMENTpy for five sites along a climate gradient in Southern California, United States, and conducted reciprocal transplant simulations analogous to a prior empirical study. The simulations demonstrated climate-dependent legacy effects of microbial communities on plant litter decomposition across the gradient. This result is consistent with the previous empirical study across the same gradient. An analysis of community-level traits further suggests that a 3-way tradeoff among resource acquisition, stress tolerance, and yield strategies influences community assembly. Simulated litter decomposition was predictable with two community traits (indicative of two of the three strategies) plus local environment, regardless of the system state (transient vs. equilibrium). Although more empirical confirmation is still needed, community traits plus local environmental factors (e.g., environment and litter chemistry) may robustly predict litter decomposition across spatial-temporal scales. In conclusion, this study offers a potential trait-based explanation for climate-dependent community effects on litter decomposition with implications for improved understanding of whole-ecosystem functioning across scales.

The effects of pollinator diversity on pollination function.

Pollination is a key ecological function of most terrestrial ecosystems. Decades of research on single-trophic-level communities, particularly plant communities, have helped to build the foundation of diversity-function theory. Yet as it stands, this theory appears to be less useful for intertrophic-level functions such as pollination, as evidenced by empirical findings that are often inconsistent with theoretical expectations. In this review, we evaluate how canonical diversity-function theory has been applied to pollination function, focusing on empirical studies of the mechanisms that drive pollinator diversity-function relationships. We first identified key features of pollination function that have hampered reconciliation with current theory. We then examined terminology for mechanisms used to discuss the findings from pollinator diversity-function studies that are sometimes inconsistent with established ecological concepts. We propose a revised diversity-function framework and describe two non-canonical diversity-function mechanisms that are particularly applicable to pollination. The first, "interactive functional complementarity," was identified previously but remains overlooked. The second, a new diversity-function mechanism, "functional enhancement," occurs when pollinator diversity increases within-niche activity. Finally, we discuss experimental approaches necessary to detect diversity-function effects in pollination.

Strata-dependent relationships among temperate forest structure, diversity, and growth rate along a local-scale environmental gradient

Exploring diversity-function relationships across overstory and understory strata is crucial for understanding ecological mechanisms, biodiversity conservation and forest management. In this study, we aimed to investigate the relationships among species diversity and stand structure, environmental factors, leaf area index (LAI), and the growth rate of overstory and understory strata in a mixed-broadleaf Korean Pine Forest in Northeast China. We performed structural equation models (SEMs) to evaluate the effects of environmental factors on overstory and understory species diversity, stand structure, and growth rate; the effects of overstory and understory species diversity and stand structure (total basal area, stem density, and diameter at the breast height variation) on the LAI and their respective growth rates; and the effect of overstory stratum on understory stratum species diversity, stand structure, and growth rate. Our results showed that species diversity determined the growth rate for overstory strata, while stem density was appropriate to determine understory growth rate. The integrative SEM accounted for 13, 13, 11, 8, and 7% of the variance in overstory species diversity, understory absolute growth rate, overstory absolute growth rate, understory stem density, and LAI, respectively. The diversity of overstory species had a positive direct influence on overstory growth but a negative direct effect on understory growth. Environmental factors (i.e., soil nutrients and soil moisture) positively influenced the understory growth rate but negatively influenced the overstory growth rate. Increasing understory stem density may increase the LAI; simultaneously, the LAI supported the understory growth rate. In natural forests, an arrangement between the overstory canopy and the availability of environmental resources is ideal for controlling species diversity and maximizing the productivity of both the overstory and understory strata.

Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification

Ocean-warming and acidification are predicted to reduce coral reef biodiversity, but the combined effects of these stressors on overall biodiversity are largely unmeasured. Here, we examined the individual and combined effects of elevated temperature (+2 °C) and reduced pH (-0.2 units) on the biodiversity of coral reef communities that developed on standardized sampling units over a 2-y mesocosm experiment. Biodiversity and species composition were measured using amplicon sequencing libraries targeting the cytochrome oxidase I (COI) barcoding gene. Ocean-warming significantly increased species richness relative to present-day control conditions, whereas acidification significantly reduced richness. Contrary to expectations, species richness in the combined future ocean treatment with both warming and acidification was not significantly different from the present-day control treatment. Rather than the predicted collapse of biodiversity under the dual stressors, we find significant changes in the relative abundance but not in the occurrence of species, resulting in a shuffling of coral reef community structure among the highly species-rich cryptobenthic community. The ultimate outcome of altered community structure for coral reef ecosystems will depend on species-specific ecological functions and community interactions. Given that most species on coral reefs are members of the understudied cryptobenthos, holistic research on reef communities is needed to accurately predict diversity-function relationships and ecosystem responses to future climate conditions.

Changes in host basal area explain associational resistance of mixed forests to primary pests

Tree species diversity generally has positive effects on forest primary productivity and resistance to natural perturbations, but diversity-function relationships can vary with site conditions. Recently, studies in forest diversity experiments have shown that tree diversity and local climate, in particular drought intensity, interactively affect insect herbivory. On the other hand, many studies focused on the response of forests to drought in terms of tree growth but without analysing the concomitant effects on susceptibility to pests. It is of particular interest to understand the combined effects of drought and tree diversity on the growth of the host tree, since host resource concentration is a determining factor of a pest’s host choice.We used a tree diversity experiment where tree species diversity and drought conditions were both manipulated to evaluate their interactive effects on the susceptibility of maritime pine (Pinus pinaster Aït.) forests to two primary pests (i.e. infesting healthy trees): the pine stem borer (PSB) Dioryctria sylvestrella, and the pine processionary moth (PPM; a leaf chewer), Thaumetopoea pityocampa. Using structural equation models, we investigated the direct and indirect effects (i.e. mediated by host resources) of the presence of birch and drought on the total number of attacks of PPM and PSB, in the same plots and in the same year.We showed that pine-birch plots were more resistant to both PPM and PSB attacks than pine monocultures. Furthermore, we found that this associational resistance pattern was due to direct effects of birch trees on attacks, possibly related to disrupting non-host volatiles (NHVs), but also to indirect, resource-mediated effects whereby the presence of birch trees reduced the amount of host pine resources available to the pests. Drought conditions modulated birch mediated effects on resistance of maritime pine forests only for PSB attacks. Overall, our work improves our understanding of tree diversity-herbivory relationships and helps explain how climate might modulate such relationships.

The impact of intra-specific diversity in the rhizobia-legume symbiosis.

Rhizobia - nitrogen-fixing, root-nodulating bacteria - play a critical role in both plant ecosystems and sustainable agriculture. Rhizobia form intracellular infections within legumes roots where they produce plant accessible nitrogen from atmospheric nitrogen and thus reduce the reliance on industrial inputs. The rhizobia-legume symbiosis is often treated as a pairwise relationship between single genotypes, both in research and in the production of rhizobial inoculants. However in nature individual plants are infected by a high diversity of rhizobia symbionts. How this diversity affects productivity within the symbiosis is unclear. Here, we use a powerful statistical approach to assess the impact of diversity within the Rhizobium leguminosarum - clover symbiosis using a biodiversity-ecosystem function framework. Statistically, we found no significant impact of rhizobium diversity. However this relationship was weakly positive - rather than negative - indicating that there is no significant cost to increasing inoculant diversity. Productivity was influenced by the identity of the strains within an inoculant; strains with the highest individual performance showed a significant positive contribution within mixed inoculants. Overall, inoculant effectiveness was best predicted by the individual performance of the best inoculant member, and only weakly predicted by the worst performing member. Collectively, our data suggest that the Rhizobium leguminosarum - clover symbiosis displays a weak diversity-function relationship, but that inoculant performance can be improved through the inclusion of high performing strains. Given the wide environmental dependence of rhizobial inoculant quality, multi-strain inoculants could be highly successful as they increase the likelihood of including a strain well adapted to local conditions across different environments.

Linking Bacterial-Fungal Relationships to Microbial Diversity and Soil Nutrient Cycling.

ABSTRACTBiodiversity is important for supporting ecosystem functioning. To evaluate the factors contributing to the strength of microbial diversity-function relationships in complex terrestrial ecosystems, we conducted a soil survey over different habitats, including an agricultural field, forest, wetland, grassland, and desert. Soil microbial multidiversity was estimated by the combination of bacterial and fungal diversity. Soil ecosystem functions were evaluated using a multinutrient cycling index (MNC) in relation to carbon, nitrate, phosphorus, and potassium cycling. Significant positive relationships between soil multidiversity and multinutrient cycling were observed in all habitats, except the grassland and desert. Specifically, community compositions showed stronger correlations with multinutrient cycling than α-diversity, indicating the crucial role of microbial community composition differences on soil nutrient cycling. Importantly, we revealed that changes in both the neutral processes (Sloan neutral modeling) and the proportion of negative bacterial-fungal associations were linked to the magnitude and direction of the diversity-MNC relationships. The habitats less governed by neutral processes and dominated by negative bacterial-fungal associations exhibited stronger negative microbial α-diversity–MNC relationships. Our findings suggested that the balance between positive and negative bacterial-fungal associations was connected to the link between soil biodiversity and ecosystem function in complex terrestrial ecosystems. This study elucidates the potential factors influencing diversity-function relationships, thereby enabling future studies to forecast the effects of belowground biodiversity on ecosystem function.IMPORTANCE The relationships between soil biodiversity and ecosystem functions are an important yet poorly understood topic in microbial ecology. This study presents an exploratory effort to gain predictive understanding of the factors driving the relationships between microbial diversity and potential soil nutrient cycling in complex terrestrial ecosystems. Our structural equation modeling and random forest analysis revealed that the balance between positive and negative bacterial-fungal associations was clearly linked to the strength of the relationships between soil microbial diversity and multiple nutrients cycling across different habitats. This study revealed the potential factors underpinning diversity-function relationships in terrestrial ecosystems and thus helps us to manage soil microbial communities for better provisioning of key ecosystem services.