Soil biota contributions to soil aggregation

Lehmann et al, NEE 1, 1828-1835 (2017)

Humankind depends on the sustainability of soils for its survival and well-being. Threatened by a rapidly changing world, our soils suffer from degradation and biodiversity loss, making it increasingly important to understand the role of soil biodiversity in soil aggregation—a key parameter for soil sustainability. Here, we provide evidence of the contribution of soil biota to soil aggregation on macro- and microaggregate scales, and evaluate how specific traits, soil biota groups and species interactions contribute to this. We conducted a global meta-analysis comprising 279 soil biota species. Our study shows a clear positive effect of soil biota on soil aggregation, with bacteria and fungi generally appearing to be more important for soil aggregation than soil animals. Bacteria contribute strongly to both macro- and microaggregates while fungi strongly affect macroaggregation. Motility, body size and population density were important traits modulating effect sizes. Investigating species interactions across major taxonomic groups revealed their beneficial impact on soil aggregation. At the broadest level, our results highlight the need to consider biodiversity as a causal factor in soil aggregation. This will require a shift from the current management and physicochemical perspective to an approach that fully embraces the significance of soil organisms, their diversity and interactions.

Global gaps in soil biodiversity data

Cameron et al, NEE 2, 1042-1043 (2018)

Soil biodiversity represents a major terrestrial biodiversity pool, supports key ecosystem services and is under pressure from human activities1. Yet soil biodiversity has been neglected from many global biodiversity assessments and policies. This omission is undoubtedly related to the paucity of comprehensive information on soil biodiversity, particularly on larger spatial scales. Information on belowground species distributions, population trends, endemism and threats to belowground diversity is important for conservation prioritization, but is practically non-existent. As a consequence, much of our understanding of global macroecological patterns in biodiversity, as well as mapping of global biodiversity hotspots, has been based on aboveground taxa (such as plants2) and has not considered the functionally vital, but less visible, biodiversity found in soil.

A test of the hierarchical model of litter decomposition

Bradford et al, NEE 1, 1836-1845 (2017)

Our basic understanding of plant litter decomposition informs the assumptions underlying widely applied soil biogeochemical models, including those embedded in Earth system models. Confidence in projected carbon cycle–climate feedbacks therefore depends on accurate knowledge about the controls regulating the rate at which plant biomass is decomposed into products such as CO2. Here we test underlying assumptions of the dominant conceptual model of litter decomposition. The model posits that a primary control on the rate of decomposition at regional to global scales is climate (temperature and moisture), with the controlling effects of decomposers negligible at such broad spatial scales. Using a regional-scale litter decomposition experiment at six sites spanning from northern Sweden to southern France—and capturing both within and among site variation in putative controls—we find that contrary to predictions from the hierarchical model, decomposer (microbial) biomass strongly regulates decomposition at regional scales. Furthermore, the size of the microbial biomass dictates the absolute change in decomposition rates with changing climate variables. Our findings suggest the need for revision of the hierarchical model, with decomposers acting as both local- and broad-scale controls on litter decomposition rates, necessitating their explicit consideration in global biogeochemical models.

Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

Mahe et al, NEE 1, 0091 (2017)

High animal and plant richness in tropical rainforest communities has long intrigued naturalists. It is unknown if similar hyperdiversity patterns are reflected at the microbial scale with unicellular eukaryotes (protists). Here we show, using environmental metabarcoding of soil samples and a phylogeny-aware cleaning step, that protist communities in Neotropical rainforests are hyperdiverse and dominated by the parasitic Apicomplexa, which infect arthropods and other animals. These host-specific parasites potentially contribute to the high animal diversity in the forests by reducing population growth in a density-dependent manner. By contrast, too few operational taxonomic units (OTUs) of Oomycota were found to broadly drive high tropical tree diversity in a host-specific manner under the Janzen-Connell model. Extremely high OTU diversity and high heterogeneity between samples within the same forests suggest that protists, not arthropods, are the most diverse eukaryotes in tropical rainforests. Our data show that protists play a large role in tropical terrestrial ecosystems long viewed as being dominated by macroorganisms.

The influence of soil communities on the temperature sensitivity of soil respiration

Johnston & Sibly, NEE 2, 1597-1602 (2018)

Soil respiration represents a major carbon flux between terrestrial ecosystems and the atmosphere, and is expected to accelerate under climate warming. Despite its importance in climate change forecasts, however, our understanding of the effects of temperature on soil respiration (RS) is incomplete. Using a metabolic ecology approach we link soil biota metabolism, community composition and heterotrophic activity to predict RS rates across five biomes. We find that accounting for the ecological mechanisms underpinning decomposition processes predicts climatological RS variations observed in an independent dataset (n = 312). The importance of community composition is evident because without it RS is substantially underestimated. With increasing temperature, we predict a latitudinal increase in RS temperature sensitivity, with Q10 values ranging between 2.33 ± 0.01 in tropical forests to 2.72 ± 0.03 in tundra. This global trend has been widely observed, but has not previously been linked to soil communities.

Divergent plant–soil feedbacks could alter future elevation ranges and ecosystem dynamics

Van Nuland et al, NEE 1, 0150 (2017)

Plant–soil feedbacks (PSF) are important interactions that may influence range dynamics in a changing world. What remains largely unknown is the generality of plant–soil biotic interactions across populations and the potential role of specific soil biota, both of which are key for understanding how PSF might change future communities and ecosystems. We combined landscape-level field observations and experimental soil treatments to test whether a dominant tree alters soil environments to impact its own performance and range shifts towards higher elevations. We show: (1) soil conditioning by trees varies with elevation, (2) soil biota relate to PSF, (3) under simulated conditions, biotic PSF constrain range shifts at lower elevations but allow for expansions at higher elevations, and (4) differences in soil conditioning predict feedback outcomes in specific range-shift scenarios. These results suggest that variable plant–soil biotic interactions may influence the migration and fragmentation of tree species, and that models incorporating soil parameters will more accurately predict future species distributions.

Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil

Yao et al, NEE 2, 499-509 (2018)

Phosphorus is a scarce nutrient in many tropical ecosystems, yet how soil microbial communities cope with growth-limiting phosphorus deficiency at the gene and protein levels remains unknown. Here, we report a metagenomic and metaproteomic comparison of microbial communities in phosphorus-deficient and phosphorus-rich soils in a 17-year fertilization experiment in a tropical forest. The large-scale proteogenomics analyses provided extensive coverage of many microbial functions and taxa in the complex soil communities. A greater than fourfold increase in the gene abundance of 3-phytase was the strongest response of soil communities to phosphorus deficiency. Phytase catalyses the release of phosphate from phytate, the most recalcitrant phosphorus-containing compound in soil organic matter. Genes and proteins for the degradation of phosphorus-containing nucleic acids and phospholipids, as well as the decomposition of labile carbon and nitrogen, were also enhanced in the phosphorus-deficient soils. In contrast, microbial communities in the phosphorus-rich soils showed increased gene abundances for the degradation of recalcitrant aromatic compounds, transformation of nitrogenous compounds and assimilation of sulfur. Overall, these results demonstrate the adaptive allocation of genes and proteins in soil microbial communities in response to shifting nutrient constraints.

Red list of a black box

Phillips et al, NEE 1, 0103 (2017)

It has recently been announced that for the first time the Federal Agency for Nature Conservation (BfN) Red List (a regional red list of threatened species in Germany) includes groups of soil invertebrates, namely earthworms, millipedes and centipedes. Although these taxa already appear in very small numbers on other regional red lists (http://www.nationalredlist.org/) and the global IUCN Red List (http://www.iucnredlist.org/), the taxonomic bias towards more charismatic species means that these understudied soil invertebrates are under-represented. However, more worrying is the lack of information regarding the threats faced by these species. Of the 47 earthworm species assessed for the BfN Red List based on occurrence data, the most common status was Least Concern (22; although 14 of the 47 earthworm species were assessed as Extremely Rare); however, there are virtually no data on long- or short-term population trends or risks faced. For example, very little is known about the effects of human impacts, such as land-use change and climate change, on below-ground communities, especially compared with above-ground organisms, highlighting the urgent need for more information.

Unknown risks to soil biodiversity from commercial fungal inoculants

Hart et al, NEE 1, 0115 (2017)

Soil is the most biodiverse ecosystem on Earth but also the most unknown. More than any other ecosystem, soils have been impacted by humans, but consequences for soil biodiversity continue to be ignored. Microbial biofertilizers such as arbuscular mycorrhizal fungi (AMF) have been applied to soil for decades, yet their ability to improve yields is mixed. Some growers view the use of biofertilizers as a viable alternative to fertilizers. However, unlike synthetic fertilizers that are increasingly subject to strict regulation, the impact of biofertilizers on biodiversity and ecosystem function has not been assessed and regulations are lacking.

Positive selection inhibits gene mobilization and transfer in soil bacterial communities

Hall et al, NEE 1, 1348-1353 (2017)

Horizontal gene transfer (HGT) between bacterial lineages is a fundamental evolutionary process that accelerates adaptation. Sequence analyses show that conjugative plasmids are principal agents of HGT in natural communities. However, we lack understanding of how the ecology of bacterial communities and their environments affect the dynamics of plasmid-mediated gene mobilization and transfer. Here we show, in simple experimental soil bacterial communities containing a conjugative mercury resistance plasmid, the repeated, independent mobilization of transposon-borne genes from chromosome to plasmid, plasmid to chromosome and, in the absence of mercury selection, interspecific gene transfers from the chromosome of one species to the other via the plasmid. By reducing conjugation, positive selection for plasmid-encoded traits, like mercury resistance, can consequently inhibit HGT. Our results suggest that interspecific plasmid-mediated gene mobilization is most likely to occur in environments where plasmids are infectious, parasitic elements rather than those where plasmids are positively selected, beneficial elements.

Urbanization erodes ectomycorrhizal fungal diversity and may cause microbial communities to converge

Epp Schmidt et al, NEE 1, 0123 (2017)

Urbanization alters the physicochemical environment, introduces non-native species and causes ecosystem characteristics to converge. It has been speculated that these alterations contribute to loss of regional and global biodiversity, but so far most urban studies have assessed macro-organisms and reported mixed evidence for biodiversity loss. We studied five cities on three continents to assess the global convergence of urban soil microbial communities. We determined the extent to which communities of bacteria, archaea and fungi are geographically distributed, and to what extent urbanization acts as a filter on species diversity. We discovered that microbial communities in general converge, but the response differed among microbial domains; soil archaeal communities showed the strongest convergence, followed by fungi, while soil bacterial communities did not converge. Our data suggest that urban soil archaeal and bacterial communities are not vulnerable to biodiversity loss, whereas urbanization may be contributing to the global diversity loss of ectomycorrhizal fungi. Ectomycorrhizae decreased in both abundance and species richness under turf and ruderal land-uses. These data add to an emerging pattern of widespread suppression of ectomycorrhizal fungi by human land-uses that involve physical disruption of the soil, management of the plant community, or nutrient enrichment.

Palaeoclimate explains a unique proportion of the global variation in soil bacterial communities

Delgada-Baquerizo et al, NEE 1, 1339-1347 (2017)

The legacy impacts of past climates on the current distribution of soil microbial communities are largely unknown. Here, we use data from more than 1,000 sites from five separate global and regional datasets to identify the importance of palaeoclimatic conditions (Last Glacial Maximum and mid-Holocene) in shaping the current structure of soil bacterial communities in natural and agricultural soils. We show that palaeoclimate explains more of the variation in the richness and composition of bacterial communities than current climate. Moreover, palaeoclimate accounts for a unique fraction of this variation that cannot be predicted from geographical location, current climate, soil properties or plant diversity. Climatic legacies (temperature and precipitation anomalies from the present to ~20 kyr ago) probably shape soil bacterial communities both directly and indirectly through shifts in soil properties and plant communities. The ability to predict the distribution of soil bacteria from either palaeoclimate or current climate declines greatly in agricultural soils, highlighting the fact that anthropogenic activities have a strong influence on soil bacterial diversity. We illustrate how climatic legacies can help to explain the current distribution of soil bacteria in natural ecosystems and advocate that climatic legacies should be considered when predicting microbial responses to climate change.