Abstract
Wetland soils are the greatest source of nitrous oxide (N
2
O), a critical greenhouse gas and ozone depleter released by microbes. Yet, microbial players and processes underlying the N
2
O ...emissions from wetland soils are poorly understood. Using in situ N
2
O measurements and by determining the structure and potential functional of microbial communities in 645 wetland soil samples globally, we examined the potential role of archaea, bacteria, and fungi in nitrogen (N) cycling and N
2
O emissions. We show that N
2
O emissions are higher in drained and warm wetland soils, and are correlated with functional diversity of microbes. We further provide evidence that despite their much lower abundance compared to bacteria, nitrifying archaeal abundance is a key factor explaining N
2
O emissions from wetland soils globally. Our data suggest that ongoing global warming and intensifying environmental change may boost archaeal nitrifiers, collectively transforming wetland soils to a greater source of N
2
O.
Plant traits determine how individual plants cope with heterogeneous environments. Despite large variability in individual traits, trait coordination and trade-offs
result in some trait combinations ...being much more widespread than others, as revealed in the global spectrum of plant form and function (GSPFF
) and the root economics space (RES
) for aboveground and fine-root traits, respectively. Here we combine the traits that define both functional spaces. Our analysis confirms the major trends of the GSPFF and shows that the RES captures additional information. The four dimensions needed to explain the non-redundant information in the dataset can be summarized in an aboveground and a fine-root plane, corresponding to the GSPFF and the RES, respectively. Both planes display high levels of species aggregation, but the differentiation among growth forms, families and biomes is lower on the fine-root plane, which does not include any size-related trait, than on the aboveground plane. As a result, many species with similar fine-root syndromes display contrasting aboveground traits. This highlights the importance of including belowground organs to the GSPFF when exploring the interplay between different natural selection pressures and whole-plant trait integration.
Summary
Feedback between plants and soil microbial communities can be a powerful driver of vegetation dynamics. Plants elicit changes in the soil microbiome that either promote or suppress ...conspecifics at the same location, thereby regulating population density‐dependence and species co‐existence. Such effects are often attributed to the accumulation of host‐specific antagonistic or beneficial microbiota in the rhizosphere. However, the identity and host‐specificity of the microbial taxa involved are rarely empirically assessed. Here we review the evidence for host‐specificity in plant‐associated microbes and propose that specific plant–soil feedbacks can also be driven by generalists. We outline the potential mechanisms by which generalist microbial pathogens, mutualists and decomposers can generate differential effects on plant hosts and synthesize existing evidence to predict these effects as a function of plant investments into defence, microbial mutualists and dispersal. Importantly, the capacity of generalist microbiota to drive plant–soil feedbacks depends not only on the traits of individual plants but also on the phylogenetic and functional diversity of plant communities. Identifying factors that promote specialization or generalism in plant–microbial interactions and thereby modulate the impact of microbiota on plant performance will advance our understanding of the mechanisms underlying plant–soil feedback and the ways it contributes to plant co‐existence.
Interactions between communities of plants and arbuscular mycorrhizal (AM) fungi shape fundamental ecosystem properties. Experimental evidence suggests that compositional changes in plant and AM ...fungal communities should be correlated, but empirical data from natural ecosystems are scarce. We investigated the dynamics of covariation between plant and AM fungal communities during three stages of grassland succession, and the biotic and abiotic factors shaping these dynamics.
Plant communities were characterised using vegetation surveys. AM fungal communities were characterised by 454-sequencing of the small subunit rRNA gene and identification against the AM fungal reference database MaarjAM. AM fungal abundance was estimated using neutral-lipid fatty acids (NLFAs).
Multivariate correlation analysis (Procrustes) revealed a significant relationship between plant and AM fungal community composition. The strength of plant–AM fungal correlation weakened during succession following cessation of grassland management, reflecting changes in the proportion of plants exhibiting different AM status. Plant–AM fungal correlation was strong when the abundance of obligate AM plants was high, and declined as the proportion of facultative AM plants increased.
We conclude that the extent to which plants rely on AM symbiosis can determine how tightly communities of plants and AM fungi are interlinked, regulating community assembly of both symbiotic partners.
1 Arbuscular mycorrhizal (AM) fungi are obligate root symbionts that are present in most terrestrial ecosystems and have roles in plant mineral nutrition, carbon cycling and biotic interactions. In ...this work, 26 publications were surveyed that report on the occurrence of natural root-colonizing AM fungi identified using rDNA region sequences. A total of 52 host plant species were investigated. Sixteen publications provided data enabling a comparison to be made of AM fungal taxon richness and community composition across 36 host plant species and 25 locations. Ninety-five fungal taxa (small subunit rRNA gene sequence types) were involved, 49 of which were recorded from at least two study sites, and 65 from more than one host plant species. 2 The number of AM fungal taxa per host plant species differed between habitat types: a significantly higher richness was found in tropical forests (18.2 fungal taxa per plant species), followed by grasslands (8.3), temperate forests (5.6) and habitats under anthropogenic influence (arable fields and polluted sites, 5.2). 3 AM fungal communities exhibit differing compositions in broadly defined habitat types: tropical forests, temperate forests and habitats under anthropogenic influence. Grassland locations around the world host heterogeneous AM fungal communities. 4 A number of AM fungi had a global distribution, including sequence types related to the Glomus intraradiceslfasciculatum group, G. mosseae, G. sp. UY1225 and G. hoi, as well as the Glomus and Scutellospora types of unknown taxonomic affiliation. Widespread taxa occur in both natural and anthropogenic (disturbed) habitats, and may show high local abundance. However, about 50% of taxa have been recorded from only a single site. 5 The current global analysis of AM fungal communities suggests that soil microorganisms may exhibit different distribution patterns, resulting in a high variability of taxon richness and composition between particular ecosystems.
Although experiments show a positive association between vascular plant and arbuscular mycorrhizal fungal (AMF) species richness, evidence from natural ecosystems is scarce. Furthermore, there is ...little knowledge about how AMF richness varies with belowground plant richness and biomass. We examined relationships among AMF richness, above‐ and belowground plant richness, and plant root and shoot biomass in a native North American grassland. Root‐colonizing AMF richness and belowground plant richness were detected from the same bulk root samples by 454‐sequencing of the AMF SSU rRNA and plant trnL genes. In total we detected 63 AMF taxa. Plant richness was 1.5 times greater belowground than aboveground. AMF richness was significantly positively correlated with plant species richness, and more strongly with below‐ than aboveground plant richness. Belowground plant richness was positively correlated with belowground plant biomass and total plant biomass, whereas aboveground plant richness was positively correlated only with belowground plant biomass. By contrast, AMF richness was negatively correlated with belowground and total plant biomass. Our results indicate that AMF richness and plant belowground richness are more strongly related with each other and with plant community biomass than with the plant aboveground richness measures that have been almost exclusively considered to date.
Analytical methods can offer insights into the structure of biological networks, but mechanisms that determine the structure of these networks remain unclear. We conducted a synthesis based on 111 ...previously published datasets to assess a range of ecological and evolutionary mechanisms that may influence the plant-associated fungal interaction networks.
We calculated the relative host effect on fungal community composition and compared nestedness and modularity among different mycorrhizal types and endophytic fungal guilds. We also assessed how plant–fungal network structure was related to host phylogeny, environmental and sampling properties.
Orchid mycorrhizal fungal communities responded most strongly to host identity, but the effect of host was similar among all other fungal guilds. Community nestedness, which did not differ among fungal guilds, declined significantly with increasing mean annual precipitation on a global scale. Orchid and ericoid mycorrhizal fungal communities were more modular than ectomycorrhizal and root endophytic communities, with arbuscular mycorrhizal fungi in an intermediate position.
Network properties among a broad suite of plant-associated fungi were largely comparable and generally unrelated to phylogenetic distance among hosts. Instead, network metrics were predominantly affected by sampling and matrix properties, indicating the importance of study design in properly inferring ecological patterns.
Despite the important ecosystem role played by arbuscular mycorrhizal fungi (AMF), little is known about spatial and temporal variation in soil AMF communities. We used pyrosequencing to characterise ...AMF communities in soil samples (n = 44) from a natural forest ecosystem. Fungal taxa were identified by BLAST matching of reads against the MaarjAM database of AMF SSU rRNA gene diversity. Sub-sampling within our dataset and experimental shortening of a set of long reads indicated that our approaches to taxonomic identification and diversity analysis were robust to variations in pyrosequencing read length and numbers of reads per sample. Different forest plots (each 10 × 10 m and separated from one another by 30 m) contained significantly different soil AMF communities, and the pairwise similarity of communities decreased with distance up to 50 m. However, there were no significant changes in community composition between different time points in the growing season (May-September). Spatial structure in soil AMF communities may be related to the heterogeneous vegetation of the natural forest study system, while the temporal stability of communities suggests that AMF in soil represent a fairly constant local species pool from which mycorrhizae form and disband during the season.
Processes controlling the assembly of microorganism communities are poorly understood. In taxonomic groups where many organisms are only described from environmental DNA, phylogenetic relationships ...may provide a proxy for functional attributes. We used a null model approach to compare the phylogenetic diversity of arbuscular mycorrhizal (AM) fungal communities coexisting within the roots of plant individuals sampled worldwide. Parallel null models were constructed using taxon pools that were filtered according to some or all of spatial scale, ecosystem type and host plant identity. This allowed us to assess the importance of individual ecological gradients in shaping phylogenetic diversity and to identify potential mechanisms. In general, coexisting fungi were more phylogenetically clustered than the random communities defined by null models. However, clustering increased when null models incorporated large spatial scales, indicating that communities are assembled according to the dispersal ability of fungal taxa. Clustering also increased when null models incorporated a variety of ecosystems or host plant species, indicating effects of habitat filtering and mutualist partner selection at wide and local scales, respectively. We did not record phylogenetic overdispersion among coexisting fungi, providing no support for a role of limiting similarity in structuring AM fungal communities. However, the existence of significant clustering even in comparison with the finest-scale null model indicates that, in addition to larger-scale deterministic and neutral processes, the symbiosis may be further influenced by genotypic selectivity or stochastic processes at very small scales.
•Phylogenetic relationships may represent functional attributes in soil microbes.•Here, phylogenetic diversity is used to assess community assembly in AMF.•Nested null models are used to identify individual processes influencing assembly.•Dispersal limitation, habitat filtering and mutualist selection all play roles.•However, very small scale deterministic or stochastic processes are also important.
Predominant frameworks for understanding plant ecology have an aboveground bias that neglects soil micro-organisms. This is inconsistent with recent work illustrating the importance of soil microbes ...in terrestrial ecology. Microbial effects have been incorporated into plant community dynamics using ideas of niche modification and plant–soil community feedbacks. Here, we expand and integrate qualitative conceptual models of plant niche and feedback to explore implications of microbial interactions for understanding plant community ecology. At the same time we review the empirical evidence for these processes. We also consider common mycorrhizal networks, and propose that these are best interpreted within the feedback framework. Finally, we apply our integrated model of niche and feedback to understanding plant coexistence, monodominance and invasion ecology.
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