ixPREFACEreiterated throughoutthetext,as criteriaforselectingand organizingthecontents ofthisbook.Themajority of figures presented in this book appear as theywere pre-pared by their original authors in their original sources.This approach isdesigned loillustrate for thereaderthatadvancements in environ-mental microbiology are a community effort.A websitewithdownloadableartwork and answersto studyquestionsis available to instructors at www.blackwellpublishing.com/madsenI hope this book will stimulate new inquiries into what I feel is one ofthe most fascinating current areas of science.I welcome comments, sug-gestions,and feedback from readers of this book.I thank themany indi-viduals whoprovided both directand indirect sources of information andinspiration.I am particularly grateful to P.D. Butler for assistance inmanuscript preparation, to J.Yavitt who guided me to the right destina-tions in the biogeochemistry literature,andto W.C.Ghiorsefor hisunbounded enthusiasm for the art and science of microbiology.Constructivecommentsfromseveralanonymousreviewersareacknow-ledged.I also apologize for inadvertently failing to include and/oracknowledgescientificcontributionsfromfellowenvironmental micro-biologist friends and colleagues.EugeneMadsen
reiterated throughout the text, as criteria for selecting and organizing the contents of this book. The majority of figures presented in this book appear as they were prepared by their original authors in their original sources. This approach is designed to illustrate for the reader that advancements in environmental microbiology are a community effort. A website with downloadable artwork and answers to study questions is available to instructors at www.blackwellpublishing.com/madsen I hope this book will stimulate new inquiries into what I feel is one of the most fascinating current areas of science. I welcome comments, suggestions, and feedback from readers of this book. I thank the many individuals who provided both direct and indirect sources of information and inspiration. I am particularly grateful to P. D. Butler for assistance in manuscript preparation, to J. Yavitt who guided me to the right destinations in the biogeochemistry literature, and to W. C. Ghiorse for his unbounded enthusiasm for the art and science of microbiology. Constructive comments from several anonymous reviewers are acknowledged. I also apologize for inadvertently failing to include and/or acknowledge scientific contributions from fellow environmental microbiologist friends and colleagues. Eugene Madsen PREFACE ix 9781405136471_1_pre.qxd 1/15/08 9:21 Page ix
Significance, History, and Challenges ofEnvironmental MicrobiologyThis chapter is designedto instill inthe readera sense of thegoals,scope,and excitementthatpermeate thediscipline of environmental microbiology. We beginwith five core concepts thatunifythe field. These are strengthened and expanded throughout the book. Next, an overview of thesignificanceofenvironmentalmicrobiologyispresented,followedbyasynopsisofkeyscholarlyeventscontributing to environmental microbiology's rich heritage. The chapter closes by reminding thereaderofthecomplexityof Earth'sbiogeochemicalsystemsandthatstrategiesintegratinginforma-tion from many scientificdisciplines canimproveourunderstandingofbiospherefunction.I.ICORECONCEPTSCANUNIFYChapterOutlineENVIRONMENTALMICROBIOLOGYI.I Core concepts can unifyenvironmentalnvironmental microbiology is inherentlymicrobiologymultidisciplinary.Itsmanydisparateareas1.2 Synopsisofthesignificanceofenvironmentalofscienceneedtobepresented coherently.Tomicrobiologyworktowardthatsynthesis,thistextusesfive1.3Abriefhistoryofenvironmental microbiologyrecurrent core concepts to bind and organize1.4 Complexityofourworldfacts and ideas.1.5 Manydisciplines and theirintegrationCoreconcept1.Environmentalmicrobiologyis like a child's picture of a house- it has (atleast)fivesides(afloor,twoverticalsides,andtwo sloping roof pieces).Thefloor isevolution.Thewallsare thermodynamics and habitat diver-sity.The roof pieces are ecology and physiology.Tolearn environmental microbiology we mustmasteranduniteall sidesofthehouse.Core concept2.The prime directiveformicrobial lifeis survival, maintenance,generation ofadenosinetriphosphate(ATP),and sporadicgrowth (generationof new cells).Topredictandunderstand microbial processes in real-world waters, soils, sediments, and other habitats, it ishelpful to keep the prime directive in mind
1 Significance, History, and Challenges of Environmental Microbiology This chapter is designed to instill in the reader a sense of the goals, scope, and excitement that permeate the discipline of environmental microbiology. We begin with five core concepts that unify the field. These are strengthened and expanded throughout the book. Next, an overview of the significance of environmental microbiology is presented, followed by a synopsis of key scholarly events contributing to environmental microbiology’s rich heritage. The chapter closes by reminding the reader of the complexity of Earth’s biogeochemical systems and that strategies integrating information from many scientific disciplines can improve our understanding of biosphere function. 1.1 CORE CONCEPTS CAN UNIFY ENVIRONMENTAL MICROBIOLOGY Environmental microbiology is inherently multidisciplinary. Its many disparate areas of science need to be presented coherently. To work toward that synthesis, this text uses five recurrent core concepts to bind and organize facts and ideas. Core concept 1. Environmental microbiology is like a child’s picture of a house – it has (at least) five sides (a floor, two vertical sides, and two sloping roof pieces). The floor is evolution. The walls are thermodynamics and habitat diversity. The roof pieces are ecology and physiology. To learn environmental microbiology we must master and unite all sides of the house. Core concept 2. The prime directive for microbial life is survival, maintenance, generation of adenosine triphosphate (ATP), and sporadic growth (generation of new cells). To predict and understand microbial processes in real-world waters, soils, sediments, and other habitats, it is helpful to keep the prime directive in mind. Chapter 1 Outline 1.1 Core concepts can unify environmental microbiology 1.2 Synopsis of the significance of environmental microbiology 1.3 A brief history of environmental microbiology 1.4 Complexity of our world 1.5 Many disciplines and their integration 9781405136471_4_001.qxd 1/15/08 9:21 Page 1
2CHAPTERISIGNIFICANCE,HISTORY,ANDCHALLENGESOFENVIRONMENTALMICROBIOLOGYCore concept 3.There is a mechanistic series of linkages between ourplanet's habitat diversity and what is recorded in the genomes ofmicroorganisms found in the world today.Diversity in habitats is syn-onymouswithdiversityinselectivepressuresandresources.Whenoper-ated upon byforces of evolution,theresultismolecular,metabolic, andphysiological diversity found in extantmicroorganisms and recorded intheir genomes.Coreconcept4.Advancements in environmental microbiology dependupon convergent lines of independent evidence using many measurementprocedures. These include microscopy,biomarkers,model cultivatedmicroorganisms,molecularbiology,andgenomictechniques applied tolaboratory-and field-based investigations.Core concept5.Environmental microbiology isa dynamic,methods-limited discipline.Each methodologyused by environmental microbio-logists has its own setof strengths,weaknesses,and potential artifacts.As new methodologies deliver new types of information to environmentalmicrobiology,practitioners need a sound foundation that affords inter-pretation of the meaning and place of the incoming discoveries.I.2SYNOPSISOFTHESIGNIFICANCEOFENVIRONMENTALMICROBIOLOGYWith the formation of planet Earth 4.6 × 10°years ago, an uncharted seriesofphysical,chemical,biochemical,and (later)biological eventsbegantounfold. Many of these events were slow or random or improbableRegardless of the precise details of how life developed on Earth, (seeSections2.3-2.7), it is now clear thatfor~70% of life'shistory,prokar-yotes werethe sole or dominant lifeforms.Prokaryotes (Bacteria andArchaea)were (and remain)not just witnesses of geologic, atmospheric,geochemical, and climatic changes that have occurred over the eons.Prokaryotes arealso activeparticipants and causativeagentsofmanygeo-chemical reactions found in the geologic record.Admittedly,moderneukaryotes(especiallylandplants)havebeenmajorbiogeochemicalandecological players on planet Earth during the most recent1.4×1o°years.Nonetheless,today,as always,prokaryotes remain the"hostsof the planet.Prokaryotescomprise~60%ofthetotalbiomass(Whitmanetal.,1998;seeChapter4),accountforasmuchas6o%oftotalrespirationofsometerrestrial habitats (Velvis, 1997;Hanson et al.,2000),and also colonizea variety of Earth's habitats devoid of eukaryotic life due to topographic,climatic and geochemical extremes of elevation, depth,pressure,pH, salin-ity,heat, orlight.The Earth's habitats present complex gradients of environmental con-ditions that include variations in temperature, light, pH, pressure, salin-ity,and both inorganic and organic compounds.The inorganicmaterialsrange from elemental sulfur to ammonia,hydrogen gas, and methane and
Core concept 3. There is a mechanistic series of linkages between our planet’s habitat diversity and what is recorded in the genomes of microorganisms found in the world today. Diversity in habitats is synonymous with diversity in selective pressures and resources. When operated upon by forces of evolution, the result is molecular, metabolic, and physiological diversity found in extant microorganisms and recorded in their genomes. Core concept 4. Advancements in environmental microbiology depend upon convergent lines of independent evidence using many measurement procedures. These include microscopy, biomarkers, model cultivated microorganisms, molecular biology, and genomic techniques applied to laboratory- and field-based investigations. Core concept 5. Environmental microbiology is a dynamic, methodslimited discipline. Each methodology used by environmental microbiologists has its own set of strengths, weaknesses, and potential artifacts. As new methodologies deliver new types of information to environmental microbiology, practitioners need a sound foundation that affords interpretation of the meaning and place of the incoming discoveries. 1.2 SYNOPSIS OF THE SIGNIFICANCE OF ENVIRONMENTAL MICROBIOLOGY With the formation of planet Earth 4.6 × 109 years ago, an uncharted series of physical, chemical, biochemical, and (later) biological events began to unfold. Many of these events were slow or random or improbable. Regardless of the precise details of how life developed on Earth, (see Sections 2.3–2.7), it is now clear that for ~70% of life’s history, prokaryotes were the sole or dominant life forms. Prokaryotes (Bacteria and Archaea) were (and remain) not just witnesses of geologic, atmospheric, geochemical, and climatic changes that have occurred over the eons. Prokaryotes are also active participants and causative agents of many geochemical reactions found in the geologic record. Admittedly, modern eukaryotes (especially land plants) have been major biogeochemical and ecological players on planet Earth during the most recent 1.4 × 109 years. Nonetheless, today, as always, prokaryotes remain the “hosts” of the planet. Prokaryotes comprise ~60% of the total biomass (Whitman et al., 1998; see Chapter 4), account for as much as 60% of total respiration of some terrestrial habitats (Velvis, 1997; Hanson et al., 2000), and also colonize a variety of Earth’s habitats devoid of eukaryotic life due to topographic, climatic and geochemical extremes of elevation, depth, pressure, pH, salinity, heat, or light. The Earth’s habitats present complex gradients of environmental conditions that include variations in temperature, light, pH, pressure, salinity, and both inorganic and organic compounds. The inorganic materials range from elemental sulfur to ammonia, hydrogen gas, and methane and 2 CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 9781405136471_4_001.qxd 1/15/08 9:21 Page 2
3CHAPTERISIGNIFICANCE,HISTORY,ANDCHALLENGESOFENVIRONMENTAL MICROBIOLOGYTable l.1Microorganisms'unique combination of traits and their broad impact on the biosphereTraits ofmicroorganismsEcological consequences of traitsSmall sizeGeochemical cycling of elementsUbiquitous distribution throughout Earth's habitatsDetoxification of organic pollutantsHigh specific surface areasDetoxification of inorganic pollutantsPotentially high rate of metabolic activityRelease of essential limiting nutrients fromPhysiological responsivenessthe biomassin onegeneration to thenextGeneticmalleabilityMaintainingthe chemical compositionof soil,Potential rapid growth ratesediment, water, and atmosphere requiredUnrivaled nutritional diversityby other forms of lifeUnrivaled enzymatic diversitytheorganicmaterialsrangefrom celluloseto lignin,fats,proteins,lipids.nucleic acid, and humic substances (see Chapter 7).Each geochemical set-ting (e.g.,anaerobic peatlands, oceanic hydrothermal vents, soil humus,deep subsurface sediments) features its own set of resources that can bephysiologically exploited by microorganisms.The thermodynamicallygoverned interactions between these resources, their settings, micro-organismsthemselves,and3.6x1o°yearsof evolutionareprobablythesource of metabolic diversity of the microbial world.Microorganisms are the primary agents of geochemical change.Theirunique combination of traits (Table 1.1) cast microorganisms in the roleof recycling agents for thebiosphere.Enzymes accelerate reaction ratesbetween thermodynamicallyunstable substances.Perhaps themost eco-logically importanttypes of enzymatic reactions arethosethat catalyzeoxidation/reduction reactions between electron donors and electronacceptors.Theseallowmicroorganismstogeneratemetabolicenergy,sur-vive, and grow.Microorganisms procreate by carrying out complex,genetically regulated sequences of biosynthetic and assimilative intracel-lular processes. Each daughter cell has essentially the same macro-molecular and elemental composition as its parent.Thus, integratedmetabolism of all nutrients (e.g.,carbon, nitrogen, phosphorus, sulfur,oxygen,hydrogen,etc.)is implicitin microbial growth.Thisgrowthandsurvivalofmicroorganismsdrivesthegeochemicalcyclingoftheelements,detoxifies many contaminant organic and inorganic compounds, makesessential nutrients present in the biomass of one generation available tothe next, and maintains the conditionsrequired by other inhabitants ofthebiosphere(Table1.1).Processescarried outbymicroorganismsinsoilssediments,oceans,lakes,andgroundwaters haveamajorimpact on envir-onmental quality,agriculture,andglobal climatechange.Theseprocessesare also the basis for current and emerging biotechnologies with indus-trial and environmental applications (see Chapter 8).Table 1.2presents
the organic materials range from cellulose to lignin, fats, proteins, lipids, nucleic acid, and humic substances (see Chapter 7). Each geochemical setting (e.g., anaerobic peatlands, oceanic hydrothermal vents, soil humus, deep subsurface sediments) features its own set of resources that can be physiologically exploited by microorganisms. The thermodynamically governed interactions between these resources, their settings, microorganisms themselves, and 3.6 × 109 years of evolution are probably the source of metabolic diversity of the microbial world. Microorganisms are the primary agents of geochemical change. Their unique combination of traits (Table 1.1) cast microorganisms in the role of recycling agents for the biosphere. Enzymes accelerate reaction rates between thermodynamically unstable substances. Perhaps the most ecologically important types of enzymatic reactions are those that catalyze oxidation/reduction reactions between electron donors and electron acceptors. These allow microorganisms to generate metabolic energy, survive, and grow. Microorganisms procreate by carrying out complex, genetically regulated sequences of biosynthetic and assimilative intracellular processes. Each daughter cell has essentially the same macromolecular and elemental composition as its parent. Thus, integrated metabolism of all nutrients (e.g., carbon, nitrogen, phosphorus, sulfur, oxygen, hydrogen, etc.) is implicit in microbial growth. This growth and survival of microorganisms drives the geochemical cycling of the elements, detoxifies many contaminant organic and inorganic compounds, makes essential nutrients present in the biomass of one generation available to the next, and maintains the conditions required by other inhabitants of the biosphere (Table 1.1). Processes carried out by microorganisms in soils, sediments, oceans, lakes, and groundwaters have a major impact on environmental quality, agriculture, and global climate change. These processes are also the basis for current and emerging biotechnologies with industrial and environmental applications (see Chapter 8). Table 1.2 presents CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 3 Table 1.1 Microorganisms’ unique combination of traits and their broad impact on the biosphere Traits of microorganisms Small size Ubiquitous distribution throughout Earth’s habitats High specific surface areas Potentially high rate of metabolic activity Physiological responsiveness Genetic malleability Potential rapid growth rate Unrivaled nutritional diversity Unrivaled enzymatic diversity Ecological consequences of traits Geochemical cycling of elements Detoxification of organic pollutants Detoxification of inorganic pollutants Release of essential limiting nutrients from the biomass in one generation to the next Maintaining the chemical composition of soil, sediment, water, and atmosphere required by other forms of life 9781405136471_4_001.qxd 1/15/08 9:21 Page 3
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4 CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY Table 1.2 Examples of nutrient cycling and physiological processes catalyzed by microorganisms in biosphere habitats (reproduced with permission from Nature Reviews Microbiology from Madsen, E.L. 2005. Identifying microorganisms responsible for ecologically significant biogeochemical processes. Nature Rev. Microbiol. 3:439–446. Macmillan Magazines, www.nature.com/reviews) Nutrient cycle Carbon Biodegradation Process Photosynthesis Carbon respiration Cellulose decomposition Methanogenesis Aerobic methane oxidation Anaerobic methane oxidation Synthetic organic compounds Petroleum hydrocarbons Fuel additives (MTBE) Nitroaromatics Pharmaceuticals, personal care products Chlorinated solvents Nature of process Light-driven CO2 fixation into biomass Oxidation of organic C to CO2 Depolymerization, respiration Methane production Methane becomes CO2 Methane becomes CO2 Decomposition, CO2 formation Decomposition, CO2 formation Decomposition, CO2 formation Decomposition Decomposition Compounds are dechlorinated via respiration in anaerobic habitats Typical habitat FwS, Os, Ow Sl Sl FwS, Os, Sw Fw, Ow, Sl Os All habitats All habitats Gw, Sl, Sw Gw, Sl, Sw Gw, Sl, Sw Gw, Sl, Sw References Pichard et al., 1997; Partensky et al., 1999; Ting et al., 2002 Heemsbergen, 2004 Jones et al., 1998 Conrad, 1996; Schink, 1997 Segers, 1998; Bull et al., 2000 Boetius et al., 2000 Alexander, 1999; Boxall et al., 2004 Van Hamme et al., 2003 Deeb et al., 2003 Spain et al., 2000, Esteve-Núñez et al., 2001 Alexander, 1999; Ternes et al., 2004 Maymo-Gatell et al., 1997; Adrian et al., 2000 9781405136471_4_001.qxd 1/15/08 9:21 Page 4