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  • Review Article
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Embracing the unknown: disentangling the complexities of the soil microbiome

Key Points

  • Soils can contain large amounts of microbial biomass, including fungi, protists, viruses, bacteria and archaea. Most of these taxa currently remain undescribed, and have physiological and ecological attributes that are unknown.

  • Soil microbial communities are highly diverse, in part because soil environmental conditions are so heterogeneous. In a single soil there is a wide range of distinct microbial habitats that contain unique microbial assemblages.

  • Spatial variability in the structure of soil microbial communities is typically larger than the temporal variability. The composition of soil bacterial communities and the abundances of specific taxa are often predictable from soil and site characteristics, including soil pH, climate and organic carbon availability.

  • Plants can clearly have important direct or indirect effects on soil microbial communities and vice versa. However, the effects of plant species on microbial taxa are often difficult to predict a priori owing, in part, to plant associations with soil microorganisms being highly context-dependent.

  • Linking specific soil microbial processes to specific microbial taxa remains difficult. One way to tackle this problem is to use genomic data to group microbial taxa according to shared similar life-history strategies and functional attributes.

  • Given recent methodological and conceptual advances, the field is poised to rapidly advance our understanding of the soil microbiome. Promising future research directions include cultivation-based analyses of soil microbial taxa, studies of soil viruses and investigations into the importance of horizontal gene transfer in shaping the soil microbiome.

Abstract

Soil microorganisms are clearly a key component of both natural and managed ecosystems. Despite the challenges of surviving in soil, a gram of soil can contain thousands of individual microbial taxa, including viruses and members of all three domains of life. Recent advances in marker gene, genomic and metagenomic analyses have greatly expanded our ability to characterize the soil microbiome and identify the factors that shape soil microbial communities across space and time. However, although most soil microorganisms remain undescribed, we can begin to categorize soil microorganisms on the basis of their ecological strategies. This is an approach that should prove fruitful for leveraging genomic information to predict the functional attributes of individual taxa. The field is now poised to identify how we can manipulate and manage the soil microbiome to increase soil fertility, improve crop production and improve our understanding of how terrestrial ecosystems will respond to environmental change.

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Figure 1: The macroenvironments and microenvironments of soil.
Figure 2: Global microbial biomass found in soil.
Figure 3: The general structure of the bacterial, archaeal, protistan and fungal communities found in soil.
Figure 4: Biotic and abiotic factors that can influence the composition of soil bacterial communities.
Figure 5: Soil biogeochemical processes that can be modulated by the soil microbiome.
Figure 6: Grime's competitor–stress tolerator–ruderal framework applied to soil bacterial heterotrophs.

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Acknowledgements

The author would like to thank all the members of his laboratory for helpful comments on previous drafts of this manuscript. He also thanks A. Oliverio for her help with Figure 3. This manuscript could not have been written without the financial support from the National Science Foundation, USA (grants DEB 1556753, DEB 155690 and EAR 1331828).

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Glossary

Soil microbiome

A general term describing all microorganisms that can be found in soil, including archaea, bacteria, viruses, fungi, protists and other microbial eukaryotes.

Rhizosphere

The soil located in close proximity to plant roots, which typically has more plant-derived carbon and a higher microbial biomass than the surrounding non-rhizosphere or 'bulk' soil.

Soil horizons

Distinct layers in a soil depth profile that are typically defined on the basis of physical or chemical characteristics.

16S ribosomal RNA gene

(16S rRNA gene) A gene that encodes a subunit of bacterial and archaeal ribosomes, and that is commonly used for taxonomic and phylogenetic analyses of bacterial and archaeal communities.

Mycorrhizal fungi

Diverse groups of fungi that can live on or in plant roots. They extend the plant root system and often (but not always) confer benefits to the plant, including nutrient and water acquisition.

Nitrogen-fixing bacteria

Free-living or symbiotic bacteria (diazotrophs) that reduce atmospheric nitrogen gas to ammonia.

Relic DNA

DNA found in soil and other environments that is extracellular or found in cells with compromised cytoplasmic membranes, as opposed to DNA from living intact cells.

Dispersal constraints

The biotic or abiotic factors that restrict the movement of microorganisms across space.

Copiotrophic bacteria

Ruderal taxa that would be expected to preferentially consume increased quantities of labile carbon pools and have high maximum growth rates when resources are abundant.

Hydraulic conductivity

The ease with which pores of a saturated soil allow water movement.

DNRA

(Dissimilatory nitrate reduction to ammonium; also known as fermentative ammonification). A potentially important soil microbial process that, similar to denitrification, leads to nitrate reduction.

Nitrification

A process carried out by specific groups of bacteria and archaea (most of which are autotrophic) that can oxidize ammonia to nitrite or nitrate.

Heterotrophic bacteria

A general term for bacteria that cannot assimilate carbon from inorganic sources (such as carbon dioxide) and instead use organic carbon compounds for anabolism.

Methanogenesis

A metabolic process by which archaea reduce carbon dioxide or other single-carbon compounds to methane.

Stable isotope probing-based methods

Techniques that use isotopically labelled substrates (for example, 13C or 15N) to identify which microorganisms in an environmental sample are capable of taking up a given substrate and incorporating the isotopic label into their nucleic acids, proteins or membrane lipids.

Horizontal gene transfer

The movement of genes from one independent, mature organism to another (either members of the same species or different species) through conjugation, transformation or transduction.

Xenobiotic degradation

The microbial breakdown and detoxification of compounds that are man-made and do not occur naturally in nature.

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Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15, 579–590 (2017). https://doi.org/10.1038/nrmicro.2017.87

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