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ectomycorrhizal fungal taxa identified in a coniferous forest soil profile were found on root tips collected to a depth of 53 cm (Rosling et al., 2003). Two taxa were restricted to the organic horizon, while 11 were found only in the mineral soil. Soil invertebrate communities also vary with depth, particularly in the organic and upper mineral soil horizons. For example, there is a succession from litter-dwelling to soil-dwelling species of collembola at the interface between organic and mineral soil layers. Gut content analysis has shown that collembola near the top of the O horizon feed preferentially on pollen grains, while those at the bottom of this layer feed mainly on fungal material and highly decomposed organic matter (Ponge, 2000).

In arid and semiarid regions, soil biota are widely distributed as biological soil crusts (also called cryptogamic, microbiotic, microphytic crusts), which form a protective soil covering (see Fig. 11.7). Soil crusts consist of a specialized community of cyanobacteria, green and brown algae, mosses, and lichens. Sticky substances produced by crust organisms bind surface soil particles together forming a continuous layer that can reach 10 cm in thickness. Cyanobacteria in arid surface soil from the badlands in Spain were recently shown to migrate vertically to and from the soil surface in response to changing moisture conditions (Garcia-Pichel and Pringault, 2001). This ability to follow water is likely an important mechanism for long-term survival of desert soil microbial communities. Soil crusts are damaged by trampling disturbances caused by livestock grazing, tourist activities (e.g., hiking, biking), and off-road vehicle traffic. Such disturbances lead to reduced diversity of crust organisms and increased soil erosion. Seedling germination and establishment are also impacted. Crust recovery can take decades.

Most information on microbial biomass, community composition, and diversity comes from studies of surface soil. The deep subsurface environment, that region below the top few meters of soil that includes deep aquifers, caves, bedrock, and unconsolidated sediments, was once considered hostile to and devoid of living organisms. However, research over the past decade has shown that large numbers of microorganisms reside in the subsurface, often to depths of tens to hundreds of meters. Subsurface microbiology emerged as a discipline largely in response to groundwater quality issues and because recent technological and methodological advances have made possible the characterization of samples collected from deep environments. The field is becoming increasingly interdisciplinary as scientists from other disciplines (e.g., geology, hydrology, geochemistry, and environmental engineering) are becoming interested in understanding the role of microorganisms in soil genesis, contaminant degradation, maintenance of groundwater quality, and the evolution of geological formations (e.g., caves). Additionally, many novel microorganisms with unique biochemical and genetic traits have been isolated from subsurface environments, and these organisms may have important industrial and pharmaceutical uses.

Deep subsurface microbial populations are dominated by bacteria, and nearly all of the major taxonomic and physiological prokaryotic groups have been found. Bacterial densities range from less than 101 to 108 cells per gram of material,

FIGURE 11.7 Biological soil crusts. (Top) Landscape with healthy soil crusts. (Middle) Close-up of mature crusts on the Colorado Plateau, USA. (Bottom) Cyanobacteria adhered to sand grains. (Courtesy of Jayne Belnap, USGS Canyonlands Field Station, Moab, UT, USA. Used by permission.)
TABLE 11.1 Subsurface Bacterial Abundance in Shallow (<10 m) and Deep (>10m) Vadose Zone Geologic Materials (Adapted from Kieft and Brockman, 2001)

Depth (m)

Plate counts (cfu g ')

Microscopic counts (cells g ')

<10

<1 x 10'-8 x 106

7 x 106-1 x 108

>10

<1 x 10'-3 x 107

3 x 104-5 x 107

depending on the method of enumeration and the depth of sample collection (Table 11.1). Groundwaters sampled from aquifers or unconsolidated sediments have bacterial concentrations ranging from 103 to 106 cells ml-1. Microbial biomass in the deep subsurface is typically several to many orders of magnitude lower than that observed for surface soils. The level of microbial diversity is also much lower in the subsurface compared to surface soils (Zhou et al., 2004). For example, recent analysis of saturated and unsaturated subsurface soils from Virginia and Delaware indicated that molecular sequences of the bacterial community fell into 6 phylo-genetic divisions compared to 13 divisions for surface soils (Zhou et al., 2004). Subsurface bacterial communities have a high proportion of nonculturable cells, and metabolic rates are very slow compared to terrestrial surface environments (Fredrickson and Fletcher, 2001). Microbial activity at these depths is limited by water availability, temperature, and availability of energy sources. Energy sources include low-concentration organic substrates or reduced inorganic substrates such as H2, CH4, or S2. As in surface soils, the size and interconnectivity of pores is an important factor regulating microbial growth. In the subsurface environment, pores exist in unconsolidated materials or as fractures or fissures in consolidated rock. Significant microbial activity occurs in pores 0.2 to 15 ^m in size, whereas little to no activity has been observed in pores with openings of less than 0.2 ^m.

While bacteria dominate most subsurface microbial communities, protozoa and fungi have been observed at depth under certain conditions. Protozoan numbers are typically at or below the level of detection at unpolluted sites; however, large protozoan populations have been observed in the subsurface of contaminated sites (Sinclair et al., 1993). Protozoan presence may thus represent a useful indicator of environmental contamination. Protozoa have been shown to stimulate subsurface nitrification (Strauss and Dodds, 1997) and bacterial degradation of dissolved organic C (Kinner et al., 1998). Mycorrhizal hyphae (both ectomycorrhizal and arbuscular mycorrhizal taxa) associated with chaparral plants growing in southern California were recovered in fractured, granitic bedrock at depths greater than 2 m (Egerton-Warburton et al., 2003). The ability of mycorrhiza to grow and function in subsurface environments may enable plants living in dry climates to survive drought conditions by enhancing water and nutrient uptake from bedrock sources.

The study of subsurface microorganisms is transforming our ideas regarding the extent of the biosphere and the role that microorganisms have and continue to play in the evolution of the subsurface environment. As one example, scientists have recently found evidence suggesting that Lower Kane Cave in Wyoming was

FIGURE 1 1.8 Gypsum associated with biofilms containing sulfur-oxidizing bacteria in Lower Kane Cave, Wyoming, USA. (Photo courtesy Annette Engel, Louisiana State University. Used by permission.)

formed by microbial activity rather than abiotic chemical reactions as was previously thought (Fig. 11.8). Sulfur-oxidizing bacteria colonize carbonate surfaces in the cave, use hydrogen sulfide from a thermal spring as an energy source, and produce sulfuric acid as a by-product (Engel et al., 2004). The microbially produced acid facilitates the conversion of limestone to gypsum, which is subsequently more easily dissolved by water. This work has provided new insights into the role of microorganisms in cave formation and enlargement.

microscale heterogeneity in microbial populations

Intact soil is a continuum of mineral particles, organic materials, pore spaces, and organisms. The shape and arrangement of soil mineral and organic particles are such that a network of pores of various shapes and sizes exists. Between 45 and 60% of the total soil volume comprises pores that are either air or water filled depending on moisture conditions. These pores may be open and connected to adjoining pores or closed and isolated from the surrounding soil. Pores of different shapes, sizes, and degree of continuity provide a mosaic of microbial habitats with very different physical, chemical, and biological characteristics, resulting in an uneven distribution of soil organisms. Since soil organisms themselves vary in size, structural heterogeneity at this scale determines where a particular organism can reside, the degree to which its movement is restricted, and its interactions with other organisms.

The heterogeneous nature of the soil pore network plays a fundamental role in determining microbial abundance, activity, and community composition by affecting the relative proportion of air- versus water-filled pores, which in turn regulates water and nutrient availability, gas diffusion, and biotic interactions such as competition and predation. Microbial activity, measured as respiratory output (i.e., CO2 evolution), is maximized when about 60% of the total soil pore space is water filled. As soil moisture declines below this level, pores become poorly interconnected, water circulation becomes restricted, and dissolved nutrients, which are carried by the soil solution, become less available for microbial utilization. Soil drying leads to a reduction of microbial biomass, particularly in the larger pores where organisms are subjected to more frequent alterations between desiccation and wetting.

At the other extreme, when most or all of the pores are filled with water, oxygen becomes limiting since diffusion rates are significantly greater in air than through water. Gas diffusion into micropores is particularly slow since small pores often retain water even under dry conditions. Restricted oxygen diffusion into micropores combined with biological oxygen consumption during the decomposition of organic matter can lead to the rapid development and persistence of anaerobic conditions. Thus survival of soil biota residing in small pores depends on their ability to carry out anaerobic respiration (e.g., denitrification), replacing oxygen with an alternative electron acceptor (e.g., NO3).

Soil bacteria range in size from small "dwarf' cells (<0.1 pm3) to large cells greater than 0.2 pm3. Small cells make up the vast majority of cell numbers (>80%); however, large cells account for most (85-90%) of the soil bacterial biomass (Blackwood and Paul, 2003). Bacteria can occupy both large and small soil pores; however, more than 80% of bacteria are thought to reside preferentially in small pores. The maximum diameter of pores most frequently colonized by bacteria is estimated to range from 2.5 to 9 pm for fine- and coarse-textured soils, respectively. Few bacteria have been observed to reside in pores <0.8 pm in diameter, which means that 20-50% of the total soil pore volume, depending on soil texture and the pore size distribution, cannot be accessed and utilized by the microbial community.

Electron microscopy has revealed that bacteria often occur as isolated cells or small colonies (<10 cells) associated with decaying organic matter; however, larger colonies of several 100 cells have been observed on the surface of aggregates isolated from a clayey pasture soil and in soils under native vegetation (Fig. 11.9). Bacterial cells are often embedded in mucilage, a sticky substance of bacterial origin to which clay particles attach. Clay encapsulation and residence in small pores may provide bacteria with protection against desiccation, predation, bacteriophage attack, digestion during travel through an earthworm gut, and the deleterious effects of introduced gases such as ethylene bromide, a soil fumigant.

Fungi, protozoa, and algae are found mainly in pores larger than 5 pm. Fungal hyphae are commonly observed on aggregate surfaces and typically do not enter small microaggregates (<30 pm). Like bacteria, fungal hyphae are often sheathed in extracellular mucilage, which not only serves as protection against predation and desiccation, but also is a gluing agent in the soil aggregation process. Mycelial fungi develop extensive hyphal networks and as they grow through the soil and

FIGURE 11.9 (Top) Bacteria on the surface of an aggregate isolated from a grassland soil. (Bottom) An amoeba with its extended pseudopodia engulfing bacteria. (Photos courtesy of V. V. S. R. Gupta, CSIRO Land and Water, Glen Osmond, South Australia, Australia. Used by permission.)

over aggregate surfaces, they bind soil particles together, thereby playing an important role in the formation and stabilization of aggregates.

Soil heterogeneity indirectly influences nutrient cycling dynamics by restricting organism movement and thereby modifying the interactions between organisms. For example, small pores influence trophic relationships and nutrient mineralization by providing refuges and protection for smaller organisms, particularly bacteria, against attack from larger predators (e.g., protozoa) that are typically unable to enter smaller pores. The location of bacteria within the pore network is a key factor in their growth and activity. Bacterial populations are consistently high in small pores, but highly variable in large pores where they are vulnerable to being consumed. This may explain, in part, why introduced bacteria (e.g., Rhizobium and biocontrol organisms) often exhibit poor survival relative to indigenous bacteria. When they are introduced in such a way as to be transported by water movement into small, protected pores, their ability to persist is enhanced. This example stresses the importance of considering soil structure and microscale heterogeneity when studying the distribution of soil organisms.

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