MICROBIAL DIVERSITY Paul V. Dunlap University of Maryland Biotechnology Institute I. Introduction quires for growth, extremes of temperature, pressure, II. The Scope of Microbial Diversity salinity, or other environmental factors. III. The Biological Significance of Microbial halophile An organism requiring high levels of salts Diversity for growth. IV. A New Era in Biological Sciences heterotroph An organism that obtains its carbon from V. The ‘‘Delft School’’ of General Microbiology organic carbon compounds. VI. The ‘‘Woesean Reformation’’ of Microbiology microbe Single-celled organisms, such as bacteria, VII. Major Groups of Microbes archaea, protists, and unicellular fungi. VIII. Concluding Comments phototroph An organism utilizing the energy of light, as in sunlight, for growth. psychrophile An organism that grows better at low temperature or requires low temperature for growth. GLOSSARY aerobe An organism that utilizes or requires the pres- ence of oxygen for growth. MICROBIAL DIVERSITY can be defined as the range anaerobe An organism able to grow in the absence of different kinds of unicellular organisms, bacteria, of oxygen. archaea, protists, and fungi. Various different microbes autotroph An organism able to utilize carbon dioxide thrive throughout the biosphere, defining the limits of as its source of carbon. life and creating conditions conducive for the survival barotolerant and barophilic Able to tolerate high pres- and evolution of other living beings. The different kinds sures and growing better under high pressure. of microbes are distinguished by their differing charac- bioluminescence Light production by living or- teristics of cellular metabolism, physiology, and mor- ganisms. phology, by their various ecological distributions and chemotroph Organisms that utilize chemicals as activities, and by their distinct genomic structure, ex- sources of energy. pression, and evolution. The diversity of microbes pres- cryptoendolithic Living within the surface of rocks. ently living on earth is known to be high and is thought elective culture The provision of appropriate physical to be enormous, but the true extent of microbial diver- and chemical conditions that elicit the growth of sity is largely unknown. New molecular tools are now specific metabolic types of microbes. permitting the diversity of microbes to be explored extremophile An organism that grows better at, or re- rapidly and their evolutionary relationships and history Encyclopedia of Biodiversity, Volume 4 Copyright 2001 by Academic Press. All rights of reproduction in any form reserved. 191 192 MICROBIAL DIVERSITY to be defined. The purpose of this article is to define the functional and evolutionary foundation of the bio- the scope of, and highlight major themes in, our current sphere. understanding of microbial life and to describe recent progress in expanding knowledge of the evolution and biological significance of these organisms. II. THE SCOPE OF ‘‘The key to taking the measure of biodiversity lies in a MICROBIAL DIVERSITY downward adjustment of scale. The smaller the organism, the broader the frontier and the deeper the unmapped We live on ‘‘a microbial planet’’ (Woese, 1999) in the terrain.’’ (Wilson, 1994) ‘‘Age of Bacteria’’ (Gould, 1996). Microorganisms, the first cellular life forms, were active on earth for more than 3.0 billion years before the development of multi- I. INTRODUCTION cellular, macroscopic life forms. During that time and continuing into the present, through the invention of Rapidly accumulating evidence indicates that microbes a spectacular array of different metabolic and physiolog- most likely account for the vast majority of kinds of ical capabilities, microbes evolved to exploit the multi- organisms on earth. Microbes carry out a stunningly tude of environments and microhabitats presented by diverse array of metabolic activities, several of which the abiotic world. They thereby obtained the cellular were instrumental in creating conditions for the evolu- building materials and energy necessary for growth and tion of other life forms. Through their colonization of reproduction. In so doing, however, they progressively diverse and extreme environments, their geochemical altered the geochemical conditions of the planet, lead- cycling of matter, and their biological interactions ing to a continual development of new conditions and among themselves and with all other organisms, mi- habitats, abiotic and biotic. Those new conditions and crobes define the limits of the biosphere and perform habitats presented both challenges to survival and op- functions essential for ecosystem development and portunities to exploit, leading to continuing evolution health. However, because microorganisms are predomi- of distinct microbial types able to endure or take advan- nantly unicellular life forms that generally are smaller tage of the biogeochemical changes taking place on than can be seen with the unaided eye, they historically earth. Once cellular life began, it is likely that no place have received disproportionately little scientific atten- on earth containing the molecules and energy condu- tion compared to that given to animals and plants. This cive to life remained abiotic for long. lack of attention has begun to shift recently as awareness The evolutionary trend toward greater complexity, of the diversity of microbes and their biological impor- seen in the relatively recent appearance of multicellular tance has grown. Of the three presently recognized do- life forms (e.g., plants and animals), however, did not mains of life, two, the Bacteria and the Archaea, are cause microbes to be displaced. The appearance of entirely microbial, and the third, the Eucarya, through plants and animals did not shunt the unicellular mi- its vast array of protists and fungi, is primarily micro- crobes to forgotten corners of the biosphere to hang on bial. The essence and full scope of the diversity of mi- and eke out a marginal existence. Instead, multicellular crobes is revealed in the dramatic differences among organisms, which themselves can be viewed as highly these microorganisms in their phenotypic characteris- evolved, complex assemblages of microorganisms, have tics of cellular metabolism, physiology, and morphol- provided unicellular microbes with a wide variety of ogy, in their ecological distributions and activities, and new habitats to colonize and exploit. Consider the vari- in their genomic structure, expression, and evolution. ous microbes whose growth is favored by the different Appreciation for the true extent of microbial diversity and changing habitats provided by the growth and se- is growing rapidly through the development and use of nescence of roots, stems, leaves, flowers, and fruits dur- molecular phylogenetic approaches, which are enabling ing the life of plants. Consider the multitude of physico- rigorous analysis of the origins and evolution of micro- chemically distinct habitats of the human skin, of our bial life. In combination with classical methods of elec- mucous membranes, and the changing environments tive culture, isolation, and phenotypic analysis, the ap- of our complex intestinal system. Along with these habi- proaches of molecular phylogeny are stimulating the tats, colonized often by assemblages of several different discovery of multitudes of new microorganisms, open- kinds of microbes, consider the species-specific devel- ing up their biology for study, and providing a clear opmental and metabolic symbioses certain bacteria have understanding of the importance of microorganisms as established with plants, such as nitrogen-fixing Rhizo- MICROBIAL DIVERSITY 193 FIGURE 1 Light-micrograph of a section of the light organ of the sepiolid squid Euprymna scolopes. The animal harbors a dense population of the luminous marine bacterium Vibrio fischeri extracellularly within a ventral tissue complex, the light organ, and uses the light produced by the bacteria in predator avoidance. Reprinted from Claes and Dunlap (1999). Copyright 1999 Wiley-Liss, Inc. bium with legumes, and with animals, such as biolumi- we do, most, however, grow best at lower oxygen levels, nescent Vibrio with marine cephalopods and fishes (Fig. and anaerobic microbes of many different types require 1). Instead of passing on the torch of preeminence in the strict absence of oxygen to survive, as found, for life to the developing multicellular organisms and then example, in sediment and gut tracts. Temperatures that politely withdrawing from the life’s center stage, mi- from a human perspective are extreme—from just be- crobes were full participants and driving forces in that low the freezing point of water in some oceanic waters development, they have continued to diversify, and they and sea ice, to several degrees above its boiling point in remain fully dominant. Plants and animals provide a waters near hydrothermal vents and in hot springs—are highly visible but thin multicellular skin over a biologi- not extreme at all to the bacteria that colonize these cally rich and complex microbial world. A sense of the habitats. Indeed, water temperatures considered cold biological dominance of microbes is given by estimates for humans (i.e., 15ЊC) can be lethally hot to true cold- of the total number of living bacteria, roughly 5 ϫ 1030 loving, psychrophilic bacteria. Barotolerant and baro- cells, with a collective biomass, despite their small size, philic bacteria, active at and requiring the extremely possibly equal to that of all other life forms (Whitman