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Environmental Microbiology Alan H. Varnam BSc, PhD Consultant Microbiologist Southern Biological and Visiting Lecturer University of North London, UK Malcolm G. Evans Photographer MANSON PUBLISHING CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2000 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Version Date: 20150414 International Standard Book Number-13: 978-1-84076-548-9 (eBook - PDF) This book contains information obtained from authentic and highly regarded sources. Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for the validity of all materials or the consequences of their use. 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CCC is a not-for-profit organization that pro- vides licenses and registration for a variety of users. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com CONTENTS Preface 4 Glossary 5 Acknowledgements 6 1 Overview 7 The Nature of Microbial Communities 8 Life at Low Nutrient Concentrations: the Common Lot of Micro-organisms 16 Physicochemical Factors Affecting the Environmental Fate of Micro-organisms 18 Competitive Strategies of Micro-organisms 23 Interactions Involving Micro-organisms 25 References 27 2 Aquatic Environments 29 Microflora of the Different Aquatic Environments 30 The Marine Environment 33 The Freshwater Environment 56 References 84 3 Terrestrial Environments 87 Soil 88 Micro-organisms and Higher Plants 105 Other Terrestrial Habitats 122 References 128 4 Extreme Environments 131 High Temperature Environments 132 Extremely Acidic Environments 137 Highly Alkaline Environments 140 Non-alkaline, Highly Saline Environments 144 References 151 Appendices 152 I Development of the Microflora in a Flooded Gravel Pit 152 II The Great Goldmine Mystery 153 III A Comparison of the Microbiological Profile of the Soil on Two Sides of a Valley 154 Further Reading 155 PREFACE Adam had ’em micro-organisms have long been exploited, The world’s shortest poem: on the antiquity of knowingly or unknowingly, in the management of microbes Planet Earth and in the economic activities of humans. Our increased understanding of the Micro-organisms are ubiquitous. They are present in interactions between micro-organisms and the the soil of our gardens, in the air that we breathe and environment have enabled a refinement of their in the sea around us. They invade and colonize our exploitation. An example is the bioremediation of bodies, both causing illness and being protective of soil polluted by oil during the Gulf War. health. They spoil our foods andyet are involved in This book is intended to provide a sound, the manufacture of some. Micro-organisms are able fundamental knowledge of environmental micro- to grow in a remarkable range of habitats, which biology, the principles being reinforced by range from the relatively hospitable, often supporting a wide range of examples, illustrated in colour a wide diversity of microbial life, to the extremely where appropriate. The interactions between the hostile, where only a single type may proliferate. An environment and the dominant microflora is example of an extremely hostile environment, which discussed as are the interactions between the various has attracted much recent interest, is the vent of components of the microflora. The emphasis, undersea volcanoes – the realm of the hyper- however, is on understanding principles. This book thermophile. Despite enormous differences in the is neither intended to be a long list of every nature and geobiology ofthe various environments, micro-organism which may be present in a given it should be appreciated that the same underlying environment, nor is it intended to provide detailed factors govern the life and death of micro-organisms descriptions of the taxonomy of the micro- irrespective of the nature of the environment. Equally, organisms. Such information, if required, may be their behaviour is governed by fundamental rules. obtained elsewhere. A vast amount of work, both at bench and As environmental microbiology is a difficult theoretical level has been necessary over a period of subject area to divide into well defined and rigid many years to enable us to assemble the body of categories, the usual chapter-based format has not knowledge concerning environmental microbiology been used. The book is divided into four main parts: available today. Until relatively recently, bench an Overview of environmental microbiology, work has been primarily based on conventional Aquatic, Terrestrial and Extreme environments, cultural techniques and, providing the inherent each subdivided into major subject areas. It is limitations are understood, these can still be of intended that this rather unconventional approach considerable value. In recent years, however, an will enhance the ease of use. Above all, however, it array of powerful new tools, many based on genetic is hoped that the book will go at least some way to or advanced microscopic techniques, have become show what a challenging and fascinating topic available. Advances at bench level have been environmental microbiology is, even when experi- complemented by the development of new concepts mental results appear to defy interpretation. at the theoretical level. The study of environmental micro-organisms is Alan H. Varnam not merely an academic pursuit. Environmental Malcolm G. Evans 4 GLOSSARY Definitions are given in the context of micro- cascade of two further anaerobic respirations, to organisms, although similar terms may be applied N gas. As part of the nitrogen cycle, it is 2 to other forms of life. important in geomicrobiology, but also occurs in nitrite-containing (cured) foods. Acidophile. A micro-organism which grows Epiphyte. A micro-organism which grows on the optimally at pH values below 5.0. Should not be surface of plants, but takes no water or nutrients confused with acid-tolerant micro-organisms. A from the plant. thermoacidophile grows both at high tempera- Eubacteria. A primary subgroup of cellular life, tures and low pH value. comprising most bacteria. Cells are prokaryotic Actinomycete. A diverse group of Gram-positive in structure, but the cell chemistry is similar to eubacteria, amongst which a mycelial growth that of eukaryotes. habit is common. Eukaryote. An organism in which the unit of Alkaliphile. A micro-organism which grows structure is the complex eukaryotic cell. optimally at pH values above 8.0. Eukarotes are of extraordinary diversity, in- Allochthonous. Micro-organisms which are not cluding all known life forms except the pro- consistently a major part of the microflora of an karyotes. environment, but which become of significance Eutrophication. The process of enrichment of a in response to an increase in nutrient concentra- body of water (usually freshwater) with in- tions, or other favourable event. Known pre- organic nutrients, such as nitrate and phosphate. viously as zymogenous. Eutrophicis the term applied to a body of water, Archaebacteria. A primary subgroup of cellular life, which has been enriched in this way. Eutrophica- comprising bacteria of prokaryotic cell structure, tion can be a natural process, but is often due to but a highly distinctive cell chemistry, which the works of man. differs profoundly from that of eubacteria. Also Hadal. The ocean deep below 11,000 m. known collectively as archaeand individually as Halophile. A micro-organism which has an obligate anarcheon. requirement for NaCl at greater than physio- Autochthonous. Micro-organisms which are con- logical levels. May be sub-classified as moderate sistently present in significant numbers in an and extreme. The term should not be applied to environment and form the indigenous micro- micro-organisms which are NaCl tolerant, but flora. which have no requirement. Haloalkilophilesare Autotroph. An organism capable of growth using halophilic micro-organisms which require a high only inorganic nutrients. Typified by green pH for growth. plants, autotrophic micro-organisms include Heterotroph. An organism, exemplified by animals, photoautotrophs(light as their energy source and which requires organic nutrients. CO as their C source) and chemoautotrophs Humus. The organic fraction of soil, consisting of 2 (chemicals as their energy source). Also known naturally occurring compounds resistant to aschemolithotrophs. degradation by micro-organisms. Bloom. Seasonal dense growth of algae or other Lichen. A composite organism consisting of a planktonic micro-organisms on water. fungus living in association with one, or some- Copiotroph. A micro-organism which requires a times two, symbionts. Symbionts may either be high level of nutrients for growth. algae or cyanobacteria. Coryneform. Gram-positive bacteria, of charac- Lithobiotic. Living in association with rocks and teristic irregular morphology, similar to that of stones.Endolithslive in the interior of stones and Corynebacterium. These are numerically impor- epilithson the surface. tant in a wide range of habitats, including soil. Methanogens. One of the constituent groups of the Cyanobacteria. Photosynthetic eubacteria, pre- archaebacteria. Anaerobic micro-organisms viously known as ‘blue-green’ algae. which convert fermentation products of other Denitrification. Anaerobic bacterial respiration of anaerobes to methane. nitrate, resulting in reduction to nitrite and, by a Methophils. A group of eubacteria having the 5 Glossary ability to use single carbon compounds, including algae, planktonic bacteria may be described as methane, as its sole source of carbon and energy. bacterioplankton, ultramicrobacteria as pico- Previously known as methylotrophs. plankton and bacteriophage as femtoplankton. Mineralization. The decomposition of plant and Zooplankton describes free floating micro- animal remains and excretion products to organisms classified with the animal kingdom. inorganic material, which may be utilized by Phytoplankton describes all photosynthetic photosynthetic organisms. planktonic organisms. Mycorrhiza. Composite structure formed by higher Prokaryote. Organisms in which the unit of struc- plant roots in symbiotic relationship with a ture is the relatively simple prokaryotic cell. fungus. These are members of two microbial groups, the Myxobacteria. The distinct group of eubacteria eubacteria and the archaebacteria. having a gliding motility and, in many cases, a Prosthecate. Bacteria characterized by the formation special developmental cycle which involves of cell extensions (prosthecae). These are filiform formation of a fruiting body. or conical, the interior being continuous with the Neuston. The layer at the surface of bodies of water. cytoplasm of the main part of the cell. Nitrate respiration. The use of nitrate in place of Rhizosphere. Regions of soil immediately surround- oxygen as the terminal electron acceptor in the ing plant roots together with the root surfaces of growth of some aerobic eubacteria. that plant. Nitrification. The geochemical process in which Saprophyte. An organism which obtains nutrients specialized eubacteria oxidize ammonia to nitrite directly from dead, or decaying, organic matter. and nitrite to nitrate. An important part of the Symbiosis A strategy for meeting biological com- nitrogen cycle. petition by adapting to life in close and con- Oligotroph. A micro-organism capable of growth tinuing association with another form of life. at low nutrient levels. Partners are known as symbionts, or bionts, e.g. Parasitism. A symbiotic relationship in which a mycobiont being a mould partner in a sym- benefit is obtained by one partner only, the biosis and a photobiont, a photosynthetic parasite. The second partner often suffers partner. damage. Stratification. Formation, in bodies of water, of Pelagic. Relating to the open sea. The term is sub- horizontal layers of distinct chemical and/or classified as epipelagic (surface waters above physical properties. The boundary is known as thermocline),mesopelagic(waters directly below the thermocline or chemocline, and stratification thermocline), bathypelagic (waters at depth ca. may either be temporary (holomitic) or per- 2,000 m) and abyssopelagic (water at depth manent (meromitic). below 3,800 m). Sulphate-reducing bacteria. Strictly anaerobic Phototroph. A photosynthetic organism, either eubacteria, capable of anaerobic respiration prokaryotic or eukaryotic. utilizing oxidized S compounds as the electron Plankton. Floating micro-organisms in aquatic acceptor. habitats. The term is not restricted to unicellular Acknowledgements The authors gratefully acknowledge the help of The libraries of the BBSRC Institute of Food many persons during the writing and preparation Research, Reading Laboratory and the University of this book. Particular thanks are due to: of Reading for their help in obtaining information. Debbie and Phil Andrews for producing many of Our colleagues, both in the UK and overseas, the hand-drawn and computer-generated drawings who have permitted us to reproduce illustrations and diagrams. derived from their research. Individual acknow- David Post of Oxoid Ltd, for the gift of selective ledgments accompany the relevant caption. media. Colleagues, both in Reading and elsewhere, for Nikon (UK) Ltd for the loan of a photographic their help and interest during the preparation of the microscope. book. 6 1 OVERVIEW Until the 1960s many aspects of environmental microbiology were dealt with on an observational basis. Certainly there was a good measure of understanding of economically important phenomena, such as the symbiotic relationship between Rhizobium and leguminous plants, while there was a basic understanding of the relationship between microbial growth and physical parameters, such as temperature and of the various types of interaction between different micro-organisms in the same environment. Overall, however, many observations remained poorly explained and, to many microbiologists, it appeared that the various paradigms used to explain and interpret the behaviour of micro-organisms in natural environments were deficient. Over the past two decades, the situation has changed and while, happily for environmental microbiologists, much remains less than fully understood, there now exists a framework of knowledge which has greatly expanded the understanding of the relationship between micro- organisms and their environments. Two examples are an understanding of biofilm formation and its environmental importance and of the survival strategies of non-endospore forming micro-organisms. 7 THE NATURE OF MICROBIAL COMMUNITIES Introduction a heterogeneous population of micro-organisms. The microbial population is organized either Natural environments are usually inhabited by horizontally or vertically depending on the direction adiverse population of micro-organisms. These can of the gradient. In many environments a wide encompass a wide range of physiological and variety of physiological and nutritional types are nutritional types, from autotrophs to heterotrophs, present and micro-organisms with apparently from psychrophiles to hyperthermophiles and from conflicting lifestyles can grow in close proximity. obligate aerobes through micro-aerophilic bacteria This is a particularly marked phenomenon in to oxygen-sensitive anaerobes. There are exceptions physically small environments where the gradients to this general rule, usually where the environment can be very steep. The oxygen gradient across small has been manipulated by man or where the extreme soil particles, for example, permits the growth of physicochemical nature limits the types able to aerobes, micro-aerophils and anaerobes within grow. Examples of the latter include highly alkaline aphysically very short distance. and saline lakes and highly acidic hot springs. Even Heterogeneous communities are of major impor- under these extreme conditions, however, diversity tance in the microbial world because of the can be much greater than was thought possible in considerable advantages gained by members of the earlier years– in recent years many other concepts population. Indeed it has been stated that spatial in environmental microbiology have been replaced. organization in biofilms and similar situations It was previously considered, for example, that permits micro-organisms to obtain many of the micro-organisms dwelt in discrete compartments benefits of multicellular life. Interaction between for each physiological and nutritional type but it is micro-organisms permits activities such as co- now recognized that most microbial ecosystems are metabolism and cross-feeding, while diverse popula- heterogeneous. More recently still, advances in tions are less affected by environmental change and methodology, in the framework of challenges to can recover from disaster more rapidly than eco- earlier orthodoxies, have gone a considerable way systems of lower diversity. This leads to long-term to elucidate the development and function of such stability, although it should be appreciated that diverse populations. most microbial ecosystems are dynamic commu- nities and are subject to continual short-term changes. Changes can result from either periodic or Spatial organization non-periodic events affecting either the physico- chemistry of the environment as a whole, or the It is now accepted that the indigenous microflora of gradients within a given environment. The physico- most environments develop in spatially organized chemical effects are both direct (through the physicochemical gradients (Keith et al., 1987); the immediate effect on a given part of the population) distance over which these gradients are generated and indirect (through the effect on interactions varies very considerably. Microbial films (biofilms) between members of the community). It may be may be only a few micrometres thick in low- considered, however, that short-term changes nutrient environments, while soil crumbs, microbial enhance long-term stability. mats, sewage flocs and biofilms in nutrient-rich environments are of macroscopic rather than micro- scopic dimensions. Less commonly, gradients may Biofilms extend over many metres. Such situations, which include stratified lakes, sewage outfalls and A number of definitions of biofilm have been geothermal springs, can be seen as exceptional but proposed. The most satisfactory is considered to be important environments. that ‘a biofilm is a community of microbes em- It is the existence of a physicochemical gradient bedded in an organic polymer matrix, adhering to that permits the development and coexistence of a surface’ (Feature 1). 8

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