Microbes are the unseen majority in soil and comprise a large portion of lifes genetic diversity. Despite their abundance, the impact of soil microbes on ecosystem processes is still poorly understood. Here we explore the various roles that soil microbes play in terrestrial ecosystems with special emphasis on their contribution to plant productivity and diversity. Soil microbes are important regulators of plant productivity, especially in nutrient poor ecosystems where plant symbionts are responsible for the acquisition of limiting nutrients. Mycorrhizal fungi and nitrogenfixing bacteria are responsible for c. 5‐20% (grassland and savannah) to 80% (temperate and boreal forests) of all nitrogen, and up to 75% of phosphorus, that is acquired by plants annually. Free-living microbes also strongly regulate plant productivity, through the mineralization of, and competition for, nutrients that sustain plant productivity. Soil microbes, including microbial pathogens, are also important regulators of plant community dynamics and plant diversity, determining plant abundance and, in some cases, facilitating invasion by exotic plants. Conservative estimates suggest that c. 20 000 plant species are completely dependent on microbial symbionts for growth and survival pointing to the importance of soil microbes as regulators of plant species richness on Earth. Overall, this review shows that soil microbes must be considered as important drivers of plant diversity and productivity in terrestrial ecosystems.

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The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems

Plant functional traits control a variety of terrestrial ecosystem processes, including soil carbon storage which is a key component of the global carbon cycle. Plant traits regulate net soil carbon storage by controlling carbon assimilation, its transfer and storage in belowground biomass, and its release from soil through respiration, fire and leaching. However, our mechanistic understanding of these processes is incomplete. Here, we present a mechanistic framework, based on the plant traits that drive soil carbon inputs and outputs, for understanding how alteration of vegetation composition will affect soil carbon sequestration under global changes. First, we show direct and indirect plant trait effects on soil carbon input and output through autotrophs and heterotrophs, and through modification of abiotic conditions, which need to be considered to determine the local carbon sequestration potential. Second, we explore how the composition of key plant traits and soil biota related to carbon input, release and storage prevail in different biomes across the globe, and address the biome-specific mechanisms by which plant trait composition may impact on soil carbon sequestration. We propose that a trait-based approach will help to develop strategies to preserve and promote carbon sequestration.

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Plant functional traits and soil carbon sequestration in contrasting biomes

The knowns, known unknowns and unknowns of sequestration of soil organic carbon

Soils harbour some of the most diverse microbiomes on Earth and are essential for both nutrient cycling and carbon storage. To understand soil functioning, it is necessary to model the global distribution patterns and functional gene repertoires of soil microorganisms, as well as the biotic and environmental associations between the diversity and structure of both bacterial and fungal soil communities1–4. Here we show, by leveraging metagenomics and metabarcoding of global topsoil samples (189 sites, 7,560 subsamples), that bacterial, but not fungal, genetic diversity is highest in temperate habitats and that microbial gene composition varies more strongly with environmental variables than with geographic distance. We demonstrate that fungi and bacteria show global niche differentiation that is associated with contrasting diversity responses to precipitation and soil pH. Furthermore, we provide evidence for strong bacterial–fungal antagonism, inferred from antibiotic-resistance genes, in topsoil and ocean habitats, indicating the substantial role of biotic interactions in shaping microbial communities. Our results suggest that both competition and environmental filtering affect the abundance, composition and encoded gene functions of bacterial and fungal communities, indicating that the relative contributions of these microorganisms to global nutrient cycling varies spatially.

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Structure and function of the global topsoil microbiome.

Over 100 gigatons of terrestrial plant biomass are produced globally each year. Ninety percent of this biomass escapes herbivory and enters the dead organic matter pool, thus supporting complex detritus-based food webs that determine the critical balance between carbon mineralization and sequestration. How will changes in biodiversity affect this vital component of ecosystem functioning? Based on our analysis of concepts and experiments of leaf decomposition in forest floors and streams, we suggest that changes in species diversity within and across trophic levels can significantly alter decomposition. This happens through various mechanisms that are broadly similar in forest floors and streams. Differences in diversity effects between these systems relate to divergent habitat conditions and evolutionary trajectories of aquatic and terrestrial decomposers.

Diversity meets decomposition

The colonization of land by plants appears to have coincided with the appearance of mycorrhiza-like fungi. Over evolutionary time, fungi have maintained their prominent role in the formation of mycorrhizal associations. In addition, however, they have been able to occupy other terrestrial niches of which the decomposition of recalcitrant organic matter is perhaps the most remarkable. This implies that, in contrast to that of aquatic organic matter decomposition, bacteria have not been able to monopolize decomposition processes in terrestrial ecosystems. The emergence of fungi in terrestrial ecosystems must have had a strong impact on the evolution of terrestrial bacteria. On the one hand, potential decomposition niches, e.g. lignin degradation, have been lost for bacteria, whereas on the other hand the presence of fungi has itself created new bacterial niches. Confrontation between bacteria and fungi is ongoing, and from studying contemporary interactions, we can learn about the impact that fungi presently have, and have had in the past, on the ecology and evolution of terrestrial bacteria. In the first part of this review, the focus is on niche differentiation between soil bacteria and fungi involved in the decomposition of plant-derived organic matter. Bacteria and fungi are seen to compete for simple plant-derived substrates and have developed antagonistic strategies. For more recalcitrant organic substrates, e.g. cellulose and lignin, both competitive and mutualistic strategies appear to have evolved. In the second part of the review, bacterial niches with respect to the utilization of fungal-derived substrates are considered. Here, several lines of development can be recognized, ranging from mutualistic exudate-consuming bacteria that are associated with fungal surfaces to endosymbiotic and mycophagous bacteria. In some cases, there are indications of fungal specific selection in fungus-associated bacteria, and possible mechanisms for such selection are discussed.

Living in a fungal world: impact of fungi on soil bacterial niche development⋆

Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil

In a previous study it was shown that the number of wood-inhabiting bacteria was drastically reduced after colonization of beech (Fagus sylvatica) wood blocks by the white-rot fungus Hypholoma fasciculare, or sulfur tuft (Folman et al. 2008). Here we report on the mechanisms of this fungal-induced antibacterial activity. Hypholoma fasciculare was allowed to invade beech and pine (Pinus sylvestris) wood blocks that had been precolonized by microorganisms from forest soil. The changes in the number of bacteria, fungal biomass, and fungal-related wood properties were followed for 23 weeks. Colonization by the fungus resulted in a rapid and large reduction in the number of bacteria (colony-forming units), which was already apparent after 4 weeks of incubation. The reduction in the number of bacteria coincided with fungal-induced acidification in both beech and pine wood blocks. No evidence was found for the involvement of toxic secondary metabolites or reactive oxygen species in the reduction of the number of bacteria. Additional experiments showed that the dominant bacteria present in the wood blocks were not able to grow under the acidic conditions (pH 3.5) created by the fungus. Hence our research pointed at rapid acidification as the major factor causing reduction of wood-inhabiting bacteria upon colonization of wood by H. fasciculare.

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Mechanism of antibacterial activity of the white-rot fungus Hypholoma fasciculare colonizing wood.

Two strains of Gram-negative, aerobic, non-pigmented, non-motile, rod-shaped bacteria were isolated from beech wood blocks during decay by the white-rot fungus Hypholoma fasciculare (Folman et al., 2008) and were designated strains BW863T and BW872. They are capable of methylotrophic growth and assimilate carbon via the ribulose-bisphosphate pathway. In addition to methanol, the novel isolates utilized ethanol, pyruvate and malate. Strains BW863T and BW872 are obligately acidophilic, mesophilic organisms capable of growth at pH values between 3.1 and 6.5 (with an optimum at pH 4.5-5.0) and at temperatures between 4 and 30 °C. Phospholipid fatty acid profiles of these bacteria contain unusually high amounts (about 90%) of 18:17c fatty acid, thereby resembling the profiles of Methylobacterium strains. The predominant quinone is Q-10. The DNA G+C content of novel isolates is 61.8-62.8 mol %. On the basis of 16S rRNA gene sequence identity, strains BW863T and BW872 are most closely related to the acidophilic methanotroph Methylocapsa acidiphila B2 (96.5-97 %). Comparative sequence analysis of mxaF, the gene encoding the large subunit of methanol dehydrogenase, placed the MxaF sequences of two novel strains in a cluster that is distinct from all previously described MxaF sequences of cultivated methylotrophs. The identity values between the MxaF sequences of the acidophilic isolates and the MxaF sequences from known alpha-, beta- and gammaproteobacterial methylotrophs comprised 69-75%, 61-63% and 64-67%, respectively. The data therefore suggest that strains BW863T and BW872 represent a novel genus and species of methylotrophic bacteria; the name Methylovirgula ligni gen. nov., sp. nov. is proposed, with strain BW863T (=DSM 19998T = NCIMB 14408T) as the type strain.

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Larissa B. Folman

Papers

Living in a fungal world: impact of fungi on soil bacterial niche development⋆

Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil

Mechanism of antibacterial activity of the white-rot fungus Hypholoma fasciculare colonizing wood.

Methylovirgula ligni gen. nov., sp. nov., an obligately acidophilic, facultatively methylotrophic bacterium with a highly divergent mxaF gene