Bacterial diversity in agroecosystems

https://doi.org/10.1016/S0167-8809(99)00030-4Get rights and content

Abstract

All life forms rely on bacterial processes for their survival. Bacterial diversity is greater than the diversity of any other group of organisms. Bacteria are responsible for diverse metabolic functions that affect soil and plant health. Nutrient cycling, organic matter formation and decomposition, soil structure formation, and plant growth promotion are among the beneficial functions that bacteria perform. Deleterious effects include plant disease promotion. As bacterial functioning is critical to soil and plant health, the objective of this manuscript was to explore bacterial diversity and bioindication in agroecosystems. Microbial research has generally involved studying bacteria that are culturable. However, it is estimated that only a small portion of all bacteria are culturable, a vast portion of soil bacterial communities remains unstudied. With molecular techniques, more information can be obtained about those bacteria that are contributing to ecosystem functioning and are viable, but not culturable. Enhancing knowledge of soil bacterial functioning and diversity will aid in the development of sustainable agroecosystems.

Introduction

Single celled organisms have been on the earth 2–3 billion years longer than any other life. Bacteria are one of the most diverse life forms on earth and may consist of more than one million species (American Society for Microbiology, 1994). More conservative estimates suggest the number of bacterial species to be over 110 000 (Hawksworth, 1991b). Only a fraction of these species has been identified, and even fewer are being studied or are in culture collections. By one estimate, only 1–10% of the earth’s bacterial species have been identified, leaving a vast portion of that biota unknown and therefore unstudied (Hawksworth, 1991a). Bacterial communities are highly diverse and are thought to exhibit greater diversity than that seen in higher orders of organisms (Torsvik et al., 1990a, Ward et al., 1992). Within bacterial populations, there is a wealth of unknown genetic information.

Bacteria have been isolated from every kind of environment including a near boiling hot spring in Yellowstone National Park (Barns et al., 1994), crude oil spills from Cook Inlet, Alaska (Rudd et al., 1996), and from Antarctica (Russell, 1971). They are responsible for many biochemical processes that are needed to sustain life (Price, 1988). Bacterial diversity provides information on life processes and evolution. By using DNA or rRNA sequence information, evolutionary relationships between different organisms can be established. These relationships may not follow traditional taxonomic hierarchies. Margulis (1992) hypothesized that molecular biological data reveals only two diverse subkingdoms of bacteria, i.e., Archaebacteria and Eubacteria. They provide sources of genetic material and function as indicators of environmental change (American Society for Microbiology, 1994). Knowledge of bacteria will increase understanding of biological interactions and aid in conservation and restoration biology. In comparisons of conventional and conservation tillage practices used on former Conservation Reserve Program (CRP) lands, fatty acid methyl ester (FAME) analyses indicated that no-till practices maintained the microbial community structure most similarly to those found in ten years of undisturbed grass (Gewin et al., 1999). Bacteria are sensitive to disturbance, such as those introduced by agriculture, pollution and other stresses (Elliott and Lynch, 1994). Understanding the effect of disturbance on soil bacterial diversity and functioning may contribute greatly to the understanding of soil quality and the development of sustainable agroecosystems (Thomas and Kevan, 1993). The purpose of this chapter is to explore the issue of bacterial diversity in ecosystems.

Bacteria are the most numerous of the microbial groups in soils, but because of their small size, 1–10 μm, it is estimated that they account for less than half of the total biomass in agricultural soils (Alexander, 1977). Bacteria are found in soil at populations of 104–109 cells g−1 soil. They are very diverse metabolically and use many different sources of energy and carbon. Bacteria traditionally have been classified in broad categories based on their principle means of obtaining carbon and energy, i.e., phototrophs, chemotrophs, autotrophs, heterotrophs or lithotrophs. Bacteria also have been characterized in broad nutritional groups and by the medium in which they grow. The use of such categories provides limited information and current divisions need to be refined (Walker, 1992, Zak et al., 1994).

Actinomycetes, a subgroup of bacteria, are found in soil at populations of 106–109 cells g−1 soil (Goodfellow et al., 1968, Kuster, 1968). The actinomycetes comprise more than 30% of the total population of microorganisms in soil; however their biomass contribution is variable and much less than that of fungi (Kuster, 1968, Gray and Williams, 1971). They are diverse metabolically and are able to use many different sources of energy and carbon (McCarthy and Williams, 1992, Holmalahti et al., 1994). Actinomycetes can be either autotrophic, heterotrophic, chemotrophic or phototrophic, and either aerobic or anaerobic. Actinomycetes play a role in the breakdown of organic material, have proteolytic activity, function in the decomposition of keratins, chitins, celluloses and starches and in nutrient cycling of amino acids and nitrogen (McCarthy and Williams, 1992; Holmalahti et al, 1994). Actinomycetes are known for producing various antibiotics which can be used to treat human and animal diseases (Nolan and Cross, 1988). They also produce chemicals which can either promote or inhibit the growth of other organisms, such as thiamine, riboflavin, flavoproteins, Vitamin B12, various porphyrin like and iron containing compounds and coenzyme A (Santos et al., 1976). In addition to antibiotic production, actinomycetes are well-known for their production of compounds responsible for the rich, earthy smell of recently plowed fields (Gerber and Lechevalier, 1965, Dionigi, 1992). Some species form actinorrhizal associations with plants and are responsible for nitrogen fixation (Davison, 1988). Mycorrhizal associations can be enhanced by the presence of actinomycetes (Carpenter-Boggs et al., 1995).

Section snippets

Functioning

Functional diversity and taxonomic diversity are often two vastly different measurements. Functional diversity includes the magnitude and capacity of soil inhabitants that are involved in key roles, such as nutrient cycling, decomposition of various compounds and other transformations (Zak et al., 1994). Taxonomic diversity usually is determined by culturability and isolation of species and may represent 10% or less of the bacteria present and active in soil. Speciation relies on

Diversity measurements

The traditional method of determining microbial diversity has been to identify to species level the culturable organisms in a soil or system and use the taxonomic differences to measure diversity (Rangaswami, 1966, Alexander, 1977). This is of limited use in that functional groups are often not represented (Zelles et al., 1995). Biomass measurements or direct counts of broad groups such as bacteria, fungi, nematodes and microarthropods can be used to compare food web structure (Ingham et al.,

Redundancy

Bacterial redundancy is thought to be a factor in bacterial functioning. It has been proposed that loss of species may not change the function of the system, biologically mediated processes or biochemical transformations (Walker, 1992). However, knowledge may be limited to only a small percentage of the characteristics of cultured bacteria (Hawksworth, 1991a) which is an even smaller percentage of the total population. Redundancy in bacterial function may not be an important issue for a high

Time and space

Temporal and spatial distribution of bacteria are factors further increasing the immensity of bacterial diversity. The diversity of soil bacteria is much greater than the diversity of above ground species, yet because of the small physical size of this group, it is much more difficult to assess. The microsite environment is the key to defining the functioning of bacterial processes (Fig. 1). Although bacteria are carried by wind and water, and for the most part, are ubiquitous, even small

Resiliency

Resiliency of an ecosystem to buffer the effects of extreme disturbances may depend in part on the diversity and interactions of the system (Perry et al., 1989, Elliott and Lynch, 1994). It may be important to monitor the diversity or possibility of these interactions as indicators of change or in response to a stress. The extinction rate of species within a system may be an important indicator of the status of the system and may be critical in determining the level of diversity necessary to

Conclusions

The enormity of bacterial diversity is incomprehensible and knowledge of the genetic diversity within the bacterial genome is limited. Bacterial diversity influences nutrient cycling and decomposition, soil structure and biological interactions. The identification of obvious bacterial functions is attainable but it is more difficult to further dissect species function and relationships. The challenge ahead is to identify the level of bacterial diversity, species composition and distribution to

Acknowledgements

Support from the USDA-ARS in cooperation with the College of Agriculture and Home Economics, Washington State University, Pullman, WA 99164 is appreciated. Trade names and company names are included for the benefit of the reader and do not imply endorsement or preferential treatment of the product by the USDA or Washington State University.

References (108)

  • N.J. Russell

    Alteration in fatty acid chain length in Micrococcus cyrophilus grown at different temperatures

    Biochim. Biophys. Acta

    (1971)
  • H.F. Stroo et al.

    Growth, survival and toxin production of root-inhibitory pseudomonads on crop residues

    Soil Biol. Biochem.

    (1988)
  • J. Swinnen et al.

    Root decay and turnover of rhizodeposits in field-grown winter wheat and spring barley estimated by 14C pulse-labelling

    Soil. Biol. Biochem.

    (1995)
  • Alexander, M., 1977. Introduction to Soil Microbiology, 2nd ed. Academic Press, New York, 467...
  • R.I. Amann et al.

    Phylogenetic identification and in situ detection of individual microbial cells without cultivation

    Microbiol. Rev.

    (1995)
  • American Society for Microbiology, 1994. Bacterial Diversity Research Priorities. American Society for Microbiology,...
  • Atlas, R.M., 1984. Use of bacterial diversity measurements to assess environmental stress. In: Klug, M.J., Reddy, C.A....
  • M.S. Aulakh et al.

    Crop residue type and placement effects on denitrification and mineralization

    Soil Sci. Soc. Am. J.

    (1991)
  • Barns, S.M., Fundyga, R.E., Jeffries, M.W., Pace, N.R., 1994. Proc. Natl. Acad. Sci. 91...
  • M.H. Beare et al.

    Residue placement and fungicide effects on fungal communities in conventional and no-tillage soils

    Soil Sci. Soc. Am. J.

    (1993)
  • L. Belser et al.

    Diversity in ammonia-oxidizing population of a soil

    Appl. Environ. Microbiol.

    (1978)
  • Bock, E., Koops, H.-P., Harms, H., 1989. Nitrifying Bacteria. In: Schlegel, H., Bowein, B.(Eds.), Autotrophic Bacteria....
  • Boddy, L., Watling, R., Lyon, A.J.E., 1988. Fungi and Ecological Disturbance, Section B. Proc. Royal Soc. Edinburgh....
  • A.T. Bull et al.

    Biodiversity as a source of innovation in biotechnology

    Annu. Rev. Microbiol.

    (1992)
  • C.A. Cambardella et al.

    Particulate soil organic matter changes across a grassland cultivation sequence

    Soil Sci. Soc. Am. J.

    (1992)
  • M. Christensen

    A view of fungal ecology

    Mycologia

    (1989)
  • H.P. Collins et al.

    Crop rotation and residue management effects on soil carbon and bacterial dynamics

    Soil Sci. Soc. Am. J.

    (1992)
  • R.J. Cook

    The influence of rotation crops on take-all decline phenomena

    Phytopathology

    (1981)
  • Cook, R.J., Baker, K.F., 1983. The Nature and Practice of Biological Control of Plant Pathogens. American...
  • Curl, E., Truelove, B., 1986. The Rhizosphere. Springer, Berlin, 288...
  • J. Davison

    Plant beneficial bacteria

    Biotechnology

    (1988)
  • DeBach, P., 1964. Biological Control Of Insect Pests and Weeds. Reinhold, New York, 844...
  • C.P. Dionigi

    Spore and geosmin production by Streptomyces tendae on several media

    J. Agric. Food Chem.

    (1992)
  • J.W. Doran

    Soil bacterial and biochemical changes associated with reduced tillage

    Soil Sci. Soc. Am. J.

    (1980)
  • E. Dorn et al.

    Isolation and characterization of a 3-chlorobenzoate degrading pseudomonad

    Arch. Microbiol.

    (1974)
  • L.F. Elliott et al.

    Pseudomonads as a factor in the growth of winter wheat (Triticum aestivum L.)

    Soil Biol. Biochem.

    (1984)
  • Elliott, L.F., Lynch, J.M., 1994. Biodiversity and soil resilience. In: Greenland, D.J., Szabolcs, I. (Eds.), Soil...
  • H.M. El Nashaar et al.

    Effect of long-term continuous cropping of spring wheat on aggressiveness of Cochliobolus sativus

    Can. J. Plant Sci.

    (1989)
  • J.K. Fredrickson et al.

    Physiological diversity and distributions of heterotrophic bacteria in deep cretaceous sediments of the Atlantic coastal plain

    Appl. Environ. Microbiol.

    (1991)
  • N.N. Gerber et al.

    Geosmin, an earthy-smelling substance isolated from actinomycetes

    Appl. Microbiol.

    (1965)
  • Gewin, V.L., Kennedy, A.C., Veseth, R., Miller, B.C., 1999. Soil quality and CRP takeout. Journal of Soil and Water...
  • C.M. Gilmour et al.

    Soil aggregation as influenced by the growth of mold species, kind in soil, and organic matter

    Soil Sci. Soc. Am. Proc.

    (1948)
  • Gochenauer, S.E., 1981. Responses of soil faunal communities to disturbance. In: Wicklow, D.T., Carroll, G.C.(Eds.),...
  • Goodfellow, M., Hill, I.R., Gray, T.R.G., 1968. Bacteria in a pine forest soil. In: Gray, T.R.G., Parkinson, D. (Eds.),...
  • Gray, T.R.G., Williams, S.T., 1971. Soil Microorganisms. Oliver & Boyd, Edinburgh, 240...
  • S.K. Haack et al.

    Accuracy, reproducibility, and interpretation of fatty acid methyl ester profiles of model bacterial communities

    Appl. Environ. Microbiol.

    (1994)
  • Hawksworth, D.L., 1991a. The Biodiversity of Microorganisms and Invertebrates: Its Role in Sustainable Agriculture. CAB...
  • M.O. Hill

    Diversity and evenness: a unifying notation and its consequences

    Ecology

    (1973)
  • P.R. Hirsch et al.

    Heavy metals from past applications of sewage sludge decrease the genetic diversity of Rhizobium leguminosarum biovar trifolii populations

    Soil Biol. Biochem.

    (1993)
  • W.E. Holben et al.

    Tracing tiny organisms

    Ecology

    (1988)
  • Cited by (0)

    View full text