Journal of Industrial Microbiology & Biotechnology (1997) 18, 302–307

 1997 Society for Industrial Microbiology 1367-5435/97/$12.00

Microbial diversity: the importance of exploration and

conservation
RR Colwell

University of Maryland Biotechnology Institute, 4321 Hartwick Road, Suite 550, College Park, MD 20740, USA

Microbial diversity is fundamental to maintenance and conservation of global genetic resources. As extreme environ-
ments are explored, the richness of microbial diversity is increasingly evident. Measures must be taken to estimate,
record, and conserve microbial diversity, not only to sustain human health but also to enrich the human condition
globally through wise use and conservation of genetic resources of the microbial world.

Keywords: microbial diversity; biodiversity conservation; marine microbial diversity

Introduction this way. Habitat protection is a means to protect organisms

and their habitats [19], a method that would be more bene-
Microorganisms—procaryotes, viruses, viroids, filamentous
ficial to protection of microbial biodiversity.
fungi, yeast, microalgae, and protozoans—comprise the
The term biodiversity, according to Erwin [20], is related
greatest numbers of individual organisms on Earth [37]. At
to the number of species, or species richness, along with
best, however, science has identified and is aware of only
‘the richness of activity each species undergoes during its
a minute fraction of them. Somewhere between 1% and
existence through events in the life of its members, plus the
0.1% of all extant bacterial species have been described
nonphenotypic expression of its genome.’ Thus, to study
[14] and the vast majority of the remaining 4 × 105 to 3 ×
microbial biodiversity, it is necessary to understand inter-
106 bacterial species [49] is unknown. Most cannot be cul-
actions between and among species in a given habitat.
tured using currently available techniques [4,13,55].
According to Erwin [20], ‘how these species are grouped
About 1% of the approximately 5 × 105 viral species has
as a living unit’ in a given ecological unit, is a task that is
been described [13], along with 5 to 10% of the approxi-
heroically difficult to complete for microorganisms, without
mately 1.5 × 106 species of fungi [43], and 4 × 104 of the
a massive, globally coordinated program of action.
approximately 1 to 2 × 105 protozoan species [49].
Microorganisms are the ubiquitous janitors of the Earth,
Viroids have been studied in an agricultural context, with
occurring in all climate areas, including those once con-
little known about occurrence of viroids in the marine
sidered to be most unlikely to support life—the cold of the
world. Obviously, this is an area ripe for exploration. The
Arctic and Antarctic, the heat of geysers and oceanic hot
protozoa merit attention, and reviews of protozoan diversity
vents, and deep within rocks. They are decomposers, con-
[21] provide information on this major grouping of micro-
verting nutrients in organic wastes and from dead organ-
organisms.
isms into molecules that are reused within ecosystems.
Yet, the natural habitats that harbor these undiscovered
Many of them live symbiotically with, in, and on higher
microorganisms are disappearing rapidly. Destruction of
organisms. Microorganisms also include agents that cause
tropical forests is estimated at between 16.4 and 20.4 × 106
disease, in some cases, maintaining ecological balance, in
hectares per year. Only a small percentage of the Earth’s
others, decimating host populations. Gold [29] suggested
temperate forests remains. The amount and quality of the
the following general rule: ‘that microbial life exists in all
world’s wetlands are in decline, and only the deepest parts
the locations where microbes can survive.’ He went on to
of the ocean appear to have maintained some degree of
state that there are no sites on Earth that have been free of
pristine quality [33].
microbial ‘infection’ for long periods of geologic time.
Microorganisms, too, are disappearing from the Earth.
Penicilliopsis clavariaeformis, which lived on a species of
Diospyros tree in Indonesia, disappeared when the tree New findings
species disappeared, as did Cookeina tricholoma, due to
Our knowledge of extant microbes is ever increasing [8]
environmental disturbances in its native Java [8].
and the range of microbial diversity has proven to be extra-
Standard policies, such as the US Endangered Species
ordinary. In the early 1980s, following the discovery of the
Act (ESA) and the Convention on International Trade in
deep sea hydrothermal vents, Stetter et al [47] identified
Endangered Species of Fauna and Flora (CITES) protect
hyperthermophilic prokaryotes from hot springs and vol-
individual species [19]. But microorganisms, especially
canic fields, as well as from shallow and abyssal marine
those we have not yet discovered, cannot be protected in
hydrothermal vents. Some of these organisms, such as the
sulfate-reducing Archaeoglobus, have been classified in the
Correspondence: Dr RR Colwell, University of Maryland Biotechnology
domain (classification higher than kingdom) Archaea [56].
Institute, 4321 Hartwick Road, Suite 550, College Park, MD 20740, USA Furthermore, representatives of the Archaea have been
Received 24 April 1996; accepted 7 January 1997 found to be widely distributed in the world oceans. Since
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303
the early identifications, many members of the Archaea nonruminant herbivores. A recently published study by Lin
have been identified and classified [55] and some produce and Stahl [34] identified a new Fibrobacter population
enzymes that have, or are expected to have, commercial within the cecum of a pony.
utility [52]. The bacterial genus Spiroplasma occurs as a symbiont
The microflora of the Antarctic has been studied inter- only within insects. Whitcomb and Hackett [54] believe
mittently since the turn of the century, but discovery and that spiroplasmas, which were identified less than 25 years
identification of cold-tolerant species of protists, cyanobac- ago, may show the greatest taxonomic diversity of all
teria, microalgae, bacteria, and yeasts have been significant microbes, another example of unusual microorganisms in
since the 1980s [23,59]. Appreciation of pyschrophiles, the new niches.
‘cold-living bacteria,’ has extended to activities of these New genera, species, and strains of fungi are being disco-
bacteria at temperatures close to freezing. Many contain vered and some are described in a recently completed book
powerful proteases active at very low temperatures. Fur- on the systematics of 900 known species within the genus
thermore, the discovery of procaryotes that have not yet Phomopsis, which lives on plant hosts and, in some circum-
been cultured, but can be detected in both the Pacific and stances, is triggered to cause disease in plants [5]. The fungi
Atlantic Oceans in large numbers opens a totally unex- have been more extensively described and characterized
plored vista. than the bacteria, with fungal species outnumbering bac-
Also, since the 1980s, knowledge of the deep terrestrial terial species more than 10-fold. Thus, investigators study-
microorganisms has increased exponentially [22]. Bacteria ing microorganisms appear to be in a race to discover more
and other microorganisms isolated from deep drilling cores species before the environments of the microorganisms
have proven to be new species with unusual physiologi- under study are forever altered or lost.
cal properties.
In the marine environment, there is some of the greatest
Microbes are necessary for life as we know it
diversity of animal and plant phyla on Earth, but this region
is the least known of all ecosystems [10]. Giovannoni et al Few individuals outside the community of microbiologists
[27], using an analysis of ribosomal RNA clones, detected discuss the conservation of species that cannot be seen
significant diversity among the bacterial picoplankton from without microscopes. Yet, microbiologists fear the possi-
the Sargasso Sea, finding a novel lineage of Sargasso Sea bility of loss of these organisms whose structure and func-
bacteria. The data support the now widely-held view that tion may never be studied before they become extinct.
microbial ecosystems contain novel, as-yet-uncultivated Because it is already known how important many micro-
species. Giovannoni et al [27] also hypothesized that viral organisms are to the health of ecosystems of the Earth, it
infections could be a contributing factor to selection pres- becomes a race with time!
sures in these species. In fact, viruses recently have been Microorganisms are the ‘janitors of the Earth,’ degrading
found to be more common in marine ecosystems than had dead organisms and recycling nutrients, making them avail-
been known previously [6,25,26,39,57,58]. It is now hypo- able for other organisms to live and grow on. They destroy
thesized that they play a significant role in the global carbon wastes and pollutants, again recycling valuable nutrients
cycle [11]. An interesting finding in the Chesapeake Bay and releasing them back into the ecosystem, or up the food
is that during late summer and early fall, viruses outnumber chain. Hawksworth and Mount [31] write, ‘Biodiversity is
bacteria [57]. consequently essential, maintaining the stability of living
Fuhrman et al [25,26] identified several unique micro- systems around us, and ensuring that we survive the death,
organism clones in marine samples collected from the west- dung, and detritus of contemporaneous members of our
ern California Current area of the Pacific Ocean and from own species as well as of other organisms.’
the Atlantic Ocean off the coast of Bermuda. These appear For example, these detritus-consuming microbes aid in
to represent new bacterial taxa, notable among them are recycling of nutrients from between 67% to 88% of the
members of the Archaea. plant material produced in deserts. Although they are aided
Coral reefs harbor abundant microbial species, some of by arthropods, nematodes, and some rodents, the micro-
which demonstrate antiviral activity [15,44,45]. In fact, the organisms are irreplaceable in the food web.
structure of marine invertebrates, eg, sponges, appears to Microorganisms live symbiotically within the guts of
comprise a structural composition dependent upon procary- higher organisms, aiding in the digestive process and in
otes. Symbioses are also a unique feature of marine bacteria fermentation of wastes [35,50]. They dwell on human and
and invertebrate animals. From these invertebrate–bacterial animal bodies and within orifices of these bodies. Most of
interactions have come some interesting new metabolites the normal flora are nonpathogenic or become pathogenic
of potential pharmaceutical value. only under specific conditions. Goatcher et al [28] studied
Previously unknown organisms comprising the the intestinal microflora of black bears (Ursus americanus),
microflora of vertebrates have recently been identified. grizzly bears (U. arctos), and the plants within their
Epulopiscium fishelsoni, the largest bacterium yet disco- environment, isolating 30 genera of bacteria and 16 genera
vered, lives within the intestinal tract of the brown sur- of fungi from grizzly bears, 28 bacterial genera and 13 fun-
geonfish, Acanthurus nigrofuscus, found in the Red Sea. gal genera from black bears, and 17 bacterial genera and
Other similar, but not as large, bacteria, are symbionts 16 fungal genera from plants.
within surgeonfish from Australia’s Great Barrier Reef [1]. Fungi and other microbes live commensally in plant root
Fibrobacter are a diverse group of fiber-digesting bacteria systems, aiding in cycling of nutrients [31]. Some fungi
found within the gastrointestinal tracts of ruminant and comprise the bottom of the food chain and are eaten by
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insects that, in turn, are eaten by higher organisms [31]. ates DNA fingerprints characteristic of the community in
Fungi and bacteria also may function as biological pest con- question. Like the rRNA gene method, this does not allow
trol agents, preventing harmful bacteria, insects, and nema- for individual identification of organisms. It does, however,
todes from destroying plants [31]. Some species of nat- allow screening and comparisons of organisms in different
urally occurring bacteria in rice fields, for example, inhibit sample areas over time.
the growth of Fusarium moniliforme, the etiologic agent of This kind of community screening, if carried out in the
bakanae disease in rice [42]. same area on a regular basis, may allow us to assess
These relatively new findings indicate the diversity and changes in microbial biodiversity at a particular site or in
essential nature of microorganisms to the biosphere. Nat- a particular ecosystem. This could constitute an early warn-
urally-occurring microorganisms can be utilized effectively ing system for environmental changes [12].
in a variety of processes and genetically-engineered micro- Others have utilized DNA reassociation rates, in which
organisms can produce useful, even essential products. denatured single-stranded DNA (ssDNA) is reassociated
Bread, wine, cheese, bean curd, soy sauce, beer, and other under conditions with controlled temperature and mono-
alcoholic beverages are all products of microbial fermen- valent cation concentration. Reassociation rates give an
tation. Without antibiotics derived from fungi and bacteria, indication of the heterogeneity of the sample [51].
most infections would be fatal. And, without industrial More specific probes and gene sequencing, along with
enzymes, many derived from microorganisms, our clothes more traditional taxonomic methods, such as phenotypic
would not be as clean, our food supply would not be as characterization, microscopy (with or without monoclonal
diverse, and we would not have ready access to inexpen- antibody tags), plating, and culturing, may be necessary to
sive, effective vitamins and pharmaceuticals. We would identify microbial species.
have no sophisticated diagnostic kits to test for disease, our One major question, however, is: Should we look solely
environment could not be cleansed, and even wars may not at taxonomic diversity, or would it be more useful to study
have been won for lack of munitions. Research supplies of function diversity? Zak et al [60] suggested that functional
RNAses, DNAses, polymerases, and other enzymes have diversity would be a better way to study the roles of micro-
even changed the legal system. organisms in the environment than looking at taxonomic
diversity. They adapted the Biolog microplate identification
system, which allows for detection of specific Gram-nega-
Techniques for studying microbial biodiversity
tive or Gram-positive bacteria on microplates, allowing
Once it is determined that an effort must be made to study study of functional diversity of bacteria in soil samples
microbial diversity, the next question is what is the best from plant community types. They did, however, point out
way to accomplish this objective? Ehrlich and Wilson [18] that this technique does not substitute for DNA or 16S
referred to bacteria as ‘a terra vitae incognita because of rRNA methods, because the Biolog system only identifies
the astonishingly small amount of research devoted to their organisms that can grow on the media. Furthermore, the
diversity, as opposed to the genetics and molecular biology Biolog system has deficiencies in identifying fresh environ-
of select species.’ Clearly, this must be changed, for all mental isolates. The question of the as-yet-unculturable
microorganisms, not just the procaryotes. microorganisms also must be considered. The study of
New techniques allow for environmental screening to functional diversity using such methods is limited, but
determine the presence of nucleic acids within environmen- development of techniques to allow both screening and
tal samples. These molecular genetic techniques allow identification for a fully complete biotic survey will be
screening of organisms that could be maintained in culture necessary.
along with those that cannot be identified by standard Viruses in marine samples can be studied by nonmolecu-
means because they cannot be cultured. Pace [4], for lar methods: transmission electron microscopy (TEM) and
example, extracted DNA directly from samples, then used epifluorescent microscopy (DAPI stain) with video [25,26]
the polymerase chain reaction (PCR) to amplify small sub- and by differential filtration [58]. The development of
unit ribosomal RNA (rRNA) genes, selectively amplifying improved methods for isolating and characterizing viruses
those found in archaea and eucarya. He and his colleagues in the marine environment now makes it possible to deter-
then compared the ribosomal DNA sequences with known mine the role of viruses in microbial communities.
rRNA sequences. Although not allowing the description of
specific organisms, this technique permits determining
Conservation initiatives
numbers and lineages of microorganisms within environ-
mental samples, notably phylogenetic relationships and Does it matter if microbial diversity is lost to incursions of
genetic similarity to sequences in established databases. humans on the environment? The answer is clearly affirm-
Although workers in many laboratories amplify 16S ative.
rRNA genes from environmental samples, and have pro- Hiding within the as-yet-undiscovered microorganisms
duced important results from such work [25,26,27], even are cures for diseases, means to clean polluted environ-
with simplification of steps, this is still a time-consuming ments, new food sources, and better ways to manufacture
technique not suitable for analysis of hundreds of samples. products used daily in modern society.
It also requires a relatively large database [14]. International guidelines and agreements include protec-
It is now possible to study microbial communities, such tion for microorganisms. Caring for the Earth [32], an
as those in the Chesapeake Bay, using the randomly-ampli- update of the World Conservation Strategy presented in
fied polymorphic DNA (RAPD) method [40]. This gener- 1980, presents a blueprint for preserving the environment
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and biological diversity. Although it does not specifically to assume that less developed nations, citing their own fin-
address the issue of preserving microbial biodiversity, it ancial problems, will follow on the path of the US.
encourages establishment of protected areas that would pro- Major ecological changes already are occurring that
tect all organisms within them, and encourages energy pro- affect the health of humans and animals worldwide.
duction from biomass, use of biological pest control, main- Baquero [3] stated, ‘A microbiologically damaged environ-
tenance of good soil conditions for agriculture, and support ment probably represents the most relevant pathogenic fac-
for taxonomic and systematics research. All of these objec- tor and consequently one of the biggest challenges in public
tives, if achieved, will have a positive impact on the study health sciences.’ Friend [24] wrote, ‘Disease is often an
and maintenance of microbial biodiversity. expression of out-of-balance systems.’
The Convention on Biodiversity, signed in Rio de
Janeiro, Brazil, in 1992, and effective December 1993,
covers microbial biodiversity and includes the Microbial
Diversity 21 initiative [30]. The General Agreement on Tar- Advantages to studying microbial biodiversity
iffs and Trade (GATT), concluded by the Uruguay Round
of Negotiations in 1994, specifically requires signatory In order to best exploit microorganisms, we need to know
nations to adopt a system of patenting for microorganisms what is there and what we can use [8]. Studies of related
[16]. The Trade-Related Intellectual Property section organisms may yield potential products. For example, spec-
(TRIPS) of GATT states that there must be intellectual pro- ies of the actinomycete Kitasatosporia have been found that
perty protection both of (genetically engineered) micro- produce a herbicide, and an antibiotic (setomimycin) [8].
organisms and microbiological processes. Microbial and fungal secondary metabolites may be sources
At the national level, initiatives may be carried out to of new chemical and pharmaceutical products [38]. Anti-
promote the conservation of microbial biodiversity. The biotics have been the major products from microbial screen-
United Kingdom, for example, is interested in decreasing ing, with some 10 000 discovered in the last 50 years [36].
the amount of land being used for intensive agriculture, More recently, microbes are being probed for compounds
setting it aside for future use. This is expected to increase with antifungal, antiviral, or antitumor activity. Other
knowledge of the microbial biodiversity of this land area drugs, like mevinolin, which reduces cholesterol in humans,
[48]. The US National Science Foundation (NSF) proposed have been found through microbial screening [36]. Fungi
a national research initiative on Biological Diversity in
are a potentially rich source of active molecules. Some
Marine Systems (BioMar) that would stimulate research in
fungi produce toxins that protect the plants on which they
systematics of marine species, including microorganisms,
live from predation [36]. Other fungi produce insect toxins
and ecosystem studies [9].
that are potential biological control agents.
Hawksworth and Mound [31] pointed out that complet-
Organisms have been found that can accumulate the
ing a worldwide inventory of biota requires additional taxo-
heavy metal gallium [8]. Microbes, especially chemolitho-
nomic collections, training of people in many different
trophic bacteria, like Thiobacillus ferroxidans, and T.
countries to carry out taxonomic studies, and serious inter-
thiooxidans, are increasingly used in mining for controlled
national coordination of these efforts. The African Network
bioleaching of metals [41]. Uses for microbes and microbial
of Microbiological Resources Centres (MIRCENs) is a step
in that direction [17]. A new MIRCEN, focusing on micro- products appear to be nearly endless. But, if many
organisms used in biohydrometallurgical processes has microbial species are lost, there is one intangible benefit
been established in Pune, India [2]. that would be lost forever: the knowledge of who we are
Not only are culture collections important, but in a world and where we came from. The remarkable discovery of the
united by electronic communication, computer databases archaea, and subsequent work with the newly discovered
may supply invaluable information to taxonomists and members of this taxon, are yielding clues to the origins of
other researchers. A move to link several microbiological life on Earth [52]. Pace (personal communication) currently
databases and add functional data to the genetic data, was is describing a new kingdom within the archaea, the Korar-
explored at the recent International Symposium on chaeota (translated as ‘the very youth of life’). Members
Microbial Ecology in Santos, Brazil [53]. of this kingdom may be the phylogenetic bridge between
the eucarya and the phylogenetically deep-rooted archaea.
Without such scanning of environmental samples for micro-
organisms, this ‘bridge group’ would remain unknown.
What is the risk if action is not taken?
Unless we find ways to continue screening and studying
There is concern within the community of microbiologists microorganisms and preserving their habitats, there is no
that, due to funding and other constraints, projects having way to know the functions of these organisms within their
immediate utility have taken priority rather than the hard natural habitats, and no way in which to understand the
work of taxonomy and microbial ecology [7]. If research evolved richness of life. A major task is to educate the
is continued in this mode, the opportunity to begin the seri- public, whose knowledge of microorganisms may be lim-
ous task of determining the presence and function of micro- ited to knowing that microorganisms can cause disease. The
organisms in the environment will be lost. At present, there public must understand that, although not ‘cuddly’ like the
are only ca 5000 nature reserves or other protected areas, panda, or as impressive as the California condor or African
comprising only 3% of the Earth’s land [46]. The trend in elephant, microorganisms are essential for the continued
the US is to decrease protected lands, and there is reason existence of human populations on Earth.
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