Micro-scale determinants of bacterial diversity in soil.
TL;DR: This review focuses on the highly heterogeneous soil matrix from the vantage point of individual bacteria and identifies how the spatial heterogeneity of soil could influence a number of ecological interactions promoting the evolution and maintenance of bacterial diversity.
Abstract: Soil habitats contain vast numbers of microorganisms and harbor a large portion of the planet's biological diversity. Although high-throughput sequencing technologies continue to advance our appreciation of this remarkable phylogenetic and functional diversity, we still have only a rudimentary understanding of the forces that allow diverse microbial populations to coexist in soils. This conspicuous knowledge gap may be partially due the human perspective from which we tend to examine soilborne microorganisms. This review focusses on the highly heterogeneous soil matrix from the vantage point of individual bacteria. Methods describing micro-scale soil habitats and their inhabitants based on sieving, dissecting, and visualizing individual soil aggregates are discussed, as are microcosm-based experiments allowing the manipulation of key soil parameters. We identify how the spatial heterogeneity of soil could influence a number of ecological interactions promoting the evolution and maintenance of bacterial diversity.
Citations
More filters
TL;DR: An overview of the importance of soil-plant-microbe interactions to the development of efficient inoculants, once PGPB are extensively studied microorganisms is presented, representing a very diverse group of easily accessible beneficial bacteria.
Abstract: Plant-microbe interactions in the rhizosphere are the determinants of plant health, productivity and soil fertility. Plant growth-promoting bacteria (PGPB) are bacteria that can enhance plant growth and protect plants from disease and abiotic stresses through a wide variety of mechanisms; those that establish close associations with plants, such as the endophytes, could be more successful in plant growth promotion. Several important bacterial characteristics, such as biological nitrogen fixation, phosphate solubilization, ACC deaminase activity, and production of siderophores and phytohormones, can be assessed as plant growth promotion (PGP) traits. Bacterial inoculants can contribute to increase agronomic efficiency by reducing production costs and environmental pollution, once the use of chemical fertilizers can be reduced or eliminated if the inoculants are efficient. For bacterial inoculants to obtain success in improving plant growth and productivity, several processes involved can influence the efficiency of inoculation, as for example the exudation by plant roots, the bacterial colonization in the roots, and soil health. This review presents an overview of the importance of soil-plant-microbe interactions to the development of efficient inoculants, once PGPB are extensively studied microorganisms, representing a very diverse group of easily accessible beneficial bacteria.
706 citations
Cites background from "Micro-scale determinants of bacteri..."
...The fine spatial heterogeneity of soils results in a complex mosaic of gradients selecting for or against bacterial growth (Vos et al., 2013)....
[...]
TL;DR: In this paper, a harmonized concept for aggregates in soils is proposed that explicitly considers the structure and build-up of microaggregates and the role of organo-mineral associations.
Abstract: All soils harbor microaggregates, i.e., compound soil structures smaller than 250 µm. These microaggregates are composed of diverse mineral, organic and biotic materials that are bound together during pedogenesis by various physical, chemical and biological processes. Consequently, microaggregates can withstand strong mechanical and physicochemical stresses and survive slaking in water, allowing them to persist in soils for several decades. Together with the physiochemical heterogeneity of their surfaces, the three-dimensional structure of microaggregates provides a large variety of ecological niches that contribute to the vast biological diversity found in soils. As reported for larger aggregate units, microaggregates are composed of smaller building units that become more complex with increasing size. In this context, organo-mineral associations can be considered structural units of soil aggregates and as nanoparticulate fractions of the microaggregates themselves. The mineral phases considered to be the most important as microaggregate forming materials are the clay minerals and Fe- and Al-(hydr)oxides. Within microaggregates, minerals are bound together primarily by physicochemical and chemical interactions involving cementing and gluing agents. The former comprise, among others, carbonates and the short-range ordered phases of Fe, Mn, and Al. The latter comprise organic materials of diverse origin and probably involve macromolecules and macromolecular mixtures. Work on microaggregate structure and development has largely focused on organic matter stability and turnover. However, little is known concerning the role microaggregates play in the fate of elements like Si, Fe, Al, P, and S. More recently, the role of microaggregates in the formation of microhabitats and the biogeography and diversity of microbial communities has been investigated. Little is known regarding how microaggregates and their properties change in time, which strongly limits our understanding of micro-scale soil structure dynamics. Similarly, only limited information is available on the mechanical stability of microaggregates, while essentially nothing is known about the flow and transport of fluids and solutes within the micro- and nanoporous microaggregate systems. Any quantitative approaches being developed for the modeling of formation, structure and properties of microaggregates are, therefore, in their infancy. We respond to the growing awareness of the importance of microaggregates for the structure, properties and functions of soils by reviewing what is currently known about the formation, composition and turnover of microaggregates. We aim to provide a better understanding of their role in soil function, and to present the major unknowns in current microaggregate research. We propose a harmonized concept for aggregates in soils that explicitly considers the structure and build-up of microaggregates and the role of organo-mineral associations. We call for experiments, studies and modeling endeavors that will link information on aggregate forming materials with their functional properties across a range of scales in order to better understand microaggregate formation and turnover. Finally, we hope to inspire a novel cohort of soil scientists that they might focus their research on improving our understanding of the role of microaggregates within the system of aggregates and so help to develop a unified and quantitative concept of aggregation processes in soils.
515 citations
Cites background from "Micro-scale determinants of bacteri..."
...This serves as one explanation for the high bacterial diversity observed in soil, which is based on coexistence in spatially separated distinct habitats (Dechesne et al., 2008; Young et al., 2008; Long and Or, 2009; Carson et al., 2010; Vos et al., 2013; Ebrahimi and Or, 2015)....
[...]
...Microorganisms are unevenly distributed in the soil matrix, indicating that some regions are more favorable and more in reach for microbial life than others (Grundmann, 2004; Nunan et al., 2007; Young et al., 2008; Vos et al., 2013)....
[...]
...Pores provide the basis for connectivity of a microhabitat as they enable the flow of water and nutrients and diffusion of gases to sustain microbial activity and enable the connection of spatially separated bacterial microcolonies so allowing interactions to occur (Vos et al., 2013)....
[...]
TL;DR: The effect of trees on the composition of microbial community was demonstrated to be stronger than other soil properties and to explain a large proportion of variation in community composition, especially in fungi.
Abstract: In forest ecosystems, trees represent the major primary producers and affect the chemical composition and microbial processes in the ecosystem via specific litter chemistry and rhizodeposition. Effects of trees on the abundance of soil microorganisms have been previously observed but the extent to which trees affect the composition of microbial communities remains unknown. Here we analyse the factors affecting the composition of bacterial and fungal communities in forest litter and soil under seven tree species studied at twenty-eight spatially independent sites of similar age developed on the same initial substrate. Microbial communities differed between litter and soil. Bacterial communities were more diverse than fungal communities, especially in litter, and exhibited higher evenness. Eighty percent of the bacterial sequences belonged to the 200–250 most dominant operational taxonomic units (OTUs), and 80% of the fungal sequences were composed of only 23–28 OTUs. The effect of tree species on the microbial-community composition was significant in both litter and soil for fungi as well as bacteria. In bacteria, the tree effect was likely partly mediated by litter and soil pH. Fungal taxa showed a greater tendency to be tree-specific: 35–37% of the dominant fungal OTUs but only 0–3% of the bacterial OTUs were restricted to 1 or 2 trees, and 15–45% of the fungi and 80% of the bacteria were common under 6 or 7 trees. Microbial taxa were demonstrated to associate with less trees than would be expected based on the patterns of their abundance in samples and the tree identity thus affects their occurrence. The numbers of observed dominant fungal OTUs in the study area increased faster with an increasing numbers of trees, indicating high β-diversity. Although the proportion of the arbuscular mycorrhizal and ectomycorrhizal fungi differed among trees, the tree-specific fungal taxa were both root-symbiotic and saprotrophic. The effect of trees on the composition of microbial community was demonstrated to be stronger than other soil properties and to explain a large proportion of variation in community composition, especially in fungi.
448 citations
TL;DR: This work provides precise data on bacterial distributions, a novel way to model them at the micrometer scale as well as some new insights on the degree of interactions between individual bacterial cells in soils.
Abstract: Despite an exceptional number of bacterial cells and species in soils, bacterial diversity seems to have little effect on soil processes, such as respiration or nitrification, that can be affected by interactions between bacterial cells. The aim of this study is to understand how bacterial cells are distributed in soil to better understand the scaling between cell-to-cell interactions and what can be measured in a few milligrams, or more, of soil. Based on the analysis of 744 images of observed bacterial distributions in soil thin sections taken at different depths, we found that the inter-cell distance was, on average 12.46 mm and that these inter-cell distances were shorter near the soil surface (10.38 mm) than at depth (.18 mm), due to changes in cell densities. These images were also used to develop a spatial statistical model, based on Log Gaussian Cox Processes, to analyse the 2D distribution of cells and construct realistic 3D bacterial distributions. Our analyses suggest that despite the very high number of cells and species in soil, bacteria only interact with a few other individuals. For example, at bacterial densities commonly found in bulk soil (10 8 cells g 21 soil), the number of neighbours a single bacterium has within an interaction distance of ca. 20 mm is relatively limited (120 cells on average). Making conservative assumptions about the distribution of species, we show that such neighbourhoods contain less than 100 species. This value did not change appreciably as a function of the overall diversity in soil, suggesting that the diversity of soil bacterial communities may be species-saturated. All in all, this work provides precise data on bacterial distributions, a novel way to model them at the micrometer scale as well as some new insights on the degree of interactions between individual bacterial cells in soils.
296 citations
TL;DR: This review explores key drivers for microbial life in soils under different climates and land-use practices at scales ranging from soil pores to landscapes and delineates special features of soil as a microbial habitat and the consequences for microbial communities.
Abstract: Soil, the living terrestrial skin of the Earth, plays a central role in supporting life and is home to an unimaginable diversity of microorganisms. This review explores key drivers for microbial life in soils under different climates and land-use practices at scales ranging from soil pores to landscapes. We delineate special features of soil as a microbial habitat (focusing on bacteria) and the consequences for microbial communities. This review covers recent modeling advances that link soil physical processes with microbial life (termed biophysical processes). Readers are introduced to concepts governing water organization in soil pores and associated transport properties and microbial dispersion ranges often determined by the spatial organization of a highly dynamic soil aqueous phase. The narrow hydrological windows of wetting and aqueous phase connectedness are crucial for resource distribution and longer range transport of microorganisms. Feedbacks between microbial activity and their immediate environment are responsible for emergence and stabilization of soil structure-the scaffolding for soil ecological functioning. We synthesize insights from historical and contemporary studies to provide an outlook for the challenges and opportunities for developing a quantitative ecological framework to delineate and predict the microbial component of soil functioning.
283 citations
Cites background from "Micro-scale determinants of bacteri..."
...evidence suggests that spatial patterns are common and are manifested at various scales (Dechesne et al. 2003; Vos et al. 2013)....
[...]
...Coexistence and diversity promoted by heterogeneity and fragmentation The physical conditions that vary with soil hydration status greatly influence microbial motility and ranges of dispersion within this patchy environment (Dechesne et al. 2010; Vos et al. 2013; Tecon and Or 2016) (Fig....
[...]
...earthworms) can mediate bacterial transport over longer distances in soil (Madsen and Alexander 1982; Vos et al. 2013)....
[...]
...A more recent (and highly recommended) review by Vos et al. (2013) has addressed microscale factors influencing bacterial diversity in soil and the experimental methods currently available to explore microhabitats....
[...]
...Although numerous studies have correctly identified the important roles of spatial and temporal microhabitat fragmentation in promoting soil microbial diversity (Or et al. 2007; Dion 2008; Vos et al. 2013), a mechanistic understanding of the processes at play remains sketchy....
[...]
References
More filters
TL;DR: In this article, the effectiveness of various binding agents at different stages in the structural organization of aggregates is described and forms the basis of a model which illustrates the architecture of an aggregate.
Abstract: Summary
The water-stability of aggregates in many soils is shown to depend on organic materials. The organic binding agents have been classified into (a) transient, mainly polysaccharides, (b), temporary, roots and fungal hyphae, and (c) persistent, resistant aromatic components associated with polyvalent metal cations, and strongly sorbed polymers. The effectiveness of various binding agents at different stages in the structural organization of aggregates is described and forms the basis of a model which illustrates the architecture of an aggregate. Roots and hyphae stabilize macro-aggregates, defined as > 250 μm diameter; consequently, macroaggregation is controlled by soil management (i.e. crop rotations), as management influences the growth of plant roots, and the oxidation of organic carbon. The water-stability of micro-aggregates depends on the persistent organic binding agents and appears to be a characteristic of the soil, independent of management.
5,389 citations
"Micro-scale determinants of bacteri..." refers background in this paper
...Micro-aggregates (< 250 lm) are generally mechanically resistant, whereas macro-aggregates (> 250 lm) are less stable and can be destroyed by soil management (Tisdall & Oades, 1982)....
[...]
TL;DR: The number of prokaryotes and the total amount of their cellular carbon on earth are estimated to be 4-6 x 10(30) cells and 350-550 Pg of C (1 Pg = 10(15) g), respectively, which is 60-100% of the estimated total carbon in plants.
Abstract: The number of prokaryotes and the total amount of their cellular carbon on earth are estimated to be 4-6 3 10 30 cells and 350-550 Pg of C (1 Pg 5 10 15 g), respectively. Thus, the total amount of prokaryotic carbon is 60-100% of the estimated total carbon in plants, and inclusion of prokaryotic carbon in global models will almost double estimates of the amount of carbon stored in living organisms. In addition, the earth's prokaryotes contain 85-130 Pg of N and 9-14 Pg of P, or about 10-fold more of these nutrients than do plants, and represent the largest pool of these nutrients in living organisms. Most of the earth's prokaryotes occur in the open ocean, in soil, and in oceanic and terrestrial subsurfaces, where the numbers of cells are 1.2 3 10 29 , 2.6 3 10 29 , 3.5 3 10 30 , and 0.25-2.5 3 10 30 , respectively. The numbers of het- erotrophic prokaryotes in the upper 200 m of the open ocean, the ocean below 200 m, and soil are consistent with average turnover times of 6-25 days, 0.8 yr, and 2.5 yr, respectively. Although subject to a great deal of uncertainty, the estimate for the average turnover time of prokaryotes in the subsurface is on the order of 1-2 3 10 3 yr. The cellular production rate for all prokaryotes on earth is estimated at 1.7 3 10 30 cellsyyr and is highest in the open ocean. The large population size and rapid growth of prokaryotes provides an enormous capacity for genetic diversity. Although invisible to the naked eye, prokaryotes are an essential component of the earth's biota. They catalyze unique and indispensable transformations in the biogeochemical cy- cles of the biosphere, produce important components of the earth's atmosphere, and represent a large portion of life's genetic diversity. Although the abundance of prokaryotes has been estimated indirectly (1, 2), the actual number of pro- karyotes and the total amount of their cellular carbon on earth have never been directly assessed. Presumably, prokaryotes' very ubiquity has discouraged investigators, because an esti- mation of the number of prokaryotes would seem to require endless cataloging of numerous habitats. To estimate the number and total carbon of prokaryotes on earth, several representative habitats were first examined. This analysis indicated that most of the prokaryotes reside in three large habitats: seawater, soil, and the sedimentysoil subsur- face. Although many other habitats contain dense populations, their numerical contribution to the total number of pro- karyotes is small. Thus, evaluating the total number and total carbon of prokaryotes on earth becomes a solvable problem. Aquatic Environments. Numerous estimates of cell density, volume, and carbon indicate that prokaryotes are ubiquitous in marine and fresh water (e.g., 3-5). Although a large range of cellular densities has been reported (10 4 -10 7 cellsyml), the
4,405 citations
"Micro-scale determinants of bacteri..." refers background in this paper
...Soils are among the most vast (Whitman et al., 1998) and biodiverse microbial habitats on Earth (Quince et al....
[...]
...Soils are among the most vast (Whitman et al., 1998) and biodiverse microbial habitats on Earth (Quince et al., 2008)....
[...]
Journal Article•
TL;DR: This stately book is to show how the various types of animals have solved the fundamental problems of life, and how their struc-ture is to be interpreted in terms of their functions and environment.
Abstract: THE aim of this stately book is to show how the various types of animals have solved the fundamental problems of life, and how their struc-ture is to be interpreted in terms of their functions and environment. The keynote of the book is to keep the gratufate the author on the success of his for he has written a worthy successor to the once-famous, now forgotten “Anatomischphysiologische Uebersicht des Tierreiches,” by Bergmann and Leuckart. The outstanding merit of the achievement is in its unified or synthetic presentation of the facts—it is at once anatomical and physiological, cecological and evolutionist. This general biological outlook is very useful for the analytic student.
4,072 citations
TL;DR: In this paper, soil organic carbon (SOC), biota, ionic bridging, clay and carbonates are associated with aggregation by rearrangement, flocculation and cementation.
3,241 citations
"Micro-scale determinants of bacteri..." refers background or methods in this paper
...To this end, a range of experimental systems are now available, each trading off biological realism with the ease by which defined (a) biotic parameters can be controlled (Bronick & Lal, 2005; Guenet et al., 2011)....
[...]
...Analysis of soil communities using sieving-based methods Physical and chemical properties of soil aggregate fractions are assumed to vary with aggregate size (Scheu et al., 1996; Kandeler et al., 2000; Six et al., 2004; Bronick & Lal, 2005)....
[...]
TL;DR: This paper advocates multifaceted approaches to the study of local adaptation, and stresses the need for experiments explicitly addressing hypotheses about the role of particular ecological and genetic factors that promote or hinder local adaptation.
Abstract: Studies of local adaptation provide important insights into the power of natural selection relative to gene flow and other evolutionary forces. They are a paradigm for testing evolutionary hypotheses about traits favoured by particular environmental factors. This paper is an attempt to summarize the conceptual framework for local adaptation studies. We first review theoretical work relevant for local adaptation. Then we discuss reciprocal transplant and common garden experiments designed to detect local adaptation in the pattern of deme · habitat interaction for fitness. Finally, we review research questions and approaches to studying the processes of local adaptation ‐ divergent natural selection, dispersal and gene flow, and other processes affecting adaptive differentiation of local demes. We advocate multifaceted approaches to the study of local adaptation, and stress the need for experiments explicitly addressing hypotheses about the role of particular ecological and genetic factors that promote or hinder local adaptation. Experimental evolution of replicated populations in controlled spatially heterogeneous environments allow direct tests of such hypotheses, and thus would be a valuable way to complement research on natural populations.
3,215 citations
"Micro-scale determinants of bacteri..." refers background in this paper
...However, although dispersal can act to match cells with their spatial niche, too much of it will randomize populations and decrease local adaptation (Kawecki & Ebert, 2004)....
[...]