10CHAPTERISIGNIFICANCE,HISTORY.AND CHALLENGESOFENVIRONMENTAL MICROBIOLOGYAsthishistoricaltreatmentInputsreaches into the twenty-first century.WaterNitrogenthe branches and traditions in en-CO2vironmental microbiology becomeSulfurso complex that patterns of indi-SunlightDustvidual contributions become diffi-cult to discern. A complete list ofschools,individual investigators,Selectedprocessesand their respective discoveries isSelectedPhotosynthesisbeyond the scope of this section.poolsRespirationTheauthor apologizesforhisGrowthCarbonDeathNitrogenbiases,limitededucation,and anyWaterN-fixationandall inadvertentomissionsthatBiomassreaders may notice in this brief his-Sulfurtorical overview.OutputsGasesWaterI.4COMPLEXITYOFOURDissolvedWORLDchemicalsEroded soilBiomassAlthough we humans are capableof developing ideas or concepts orFigure 1.3Watershed in a temperate forest ecosystem.models that partially describe theArrowsshowtheinputsand outflowsfromthesystembiosphere we live in, real-worldReservoirs for carbon, nitrogen, and other nutrients includecomplexity of ecological systemsbiomass,soil litterlayer,soilmineral layer,subsoil,snowand subsystems remains generallystreams,and lakes.Dominant physiological processesbeyond full scientific description.carriedoutbybiota includephotosynthesis,grazingFigures 1.3 and 1.4 are designed todecomposition,respiration,nitrogen fixation,begin to develop for the reader aammonification, and nitrification.Key abiotic processesinclude insolation (sunlight),transport,precipitation,sense of the complexity of real-runoff,infiltration,dissolution,andacid/baseandworld ecosystems- in this caseaoxidation/reduction reactions (seeTable1.4).Netbudgetstemperate forested watershed.Thecanbeconstructedforecosystems;when inputsmatchwatershed depicted in Figure 1.3 isoutputs, the systems are said to be"steady state".open (energy and materials flowthrough it) and features dynamicchangesintimeand space.Thewatershedsystemcontainsmany com-ponents ranging fromthesitegeologyand soilstoboth small andlargecreatures,including microorganisms.Climate-related influences aremajorvariablesthat,in turn,causevariationsin howthecreaturesandtheirhabitat interact.Biogeochemical processes aremanifestations of suchinteractions.Theseprocessesincludechemical andphysical reactions,aswell as the diverse physiological reactions and behavior (Table 1.4).Thephysical,chemical,nutritional,and ecological conditionsfor watershedinhabitantsvaryfromthe scaleofmicrometerstokilometers.Regard-ing temporal variability,in situ processes that directly and indirectly
As this historical treatment reaches into the twenty-first century, the branches and traditions in environmental microbiology become so complex that patterns of individual contributions become diffi- cult to discern. A complete list of schools, individual investigators, and their respective discoveries is beyond the scope of this section. The author apologizes for his biases, limited education, and any and all inadvertent omissions that readers may notice in this brief historical overview. 1.4 COMPLEXITY OF OUR WORLD Although we humans are capable of developing ideas or concepts or models that partially describe the biosphere we live in, real-world complexity of ecological systems and subsystems remains generally beyond full scientific description. Figures 1.3 and 1.4 are designed to begin to develop for the reader a sense of the complexity of realworld ecosystems – in this case a temperate forested watershed. The watershed depicted in Figure 1.3 is open (energy and materials flow through it) and features dynamic changes in time and space. The watershed system contains many components ranging from the site geology and soils to both small and large creatures, including microorganisms. Climate-related influences are major variables that, in turn, cause variations in how the creatures and their habitat interact. Biogeochemical processes are manifestations of such interactions. These processes include chemical and physical reactions, as well as the diverse physiological reactions and behavior (Table 1.4). The physical, chemical, nutritional, and ecological conditions for watershed inhabitants vary from the scale of micrometers to kilometers. Regarding temporal variability, in situ processes that directly and indirectly 10 CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY Photosynthesis Respiration Growth Death N-fixation Selected processes Carbon Nitrogen Water Biomass Sulfur Selected pools Gases Water Dissolved chemicals Eroded soil Biomass Outputs Water Nitrogen CO2 Sulfur Sunlight Dust Inputs Figure 1.3 Watershed in a temperate forest ecosystem. Arrows show the inputs and outflows from the system. Reservoirs for carbon, nitrogen, and other nutrients include biomass, soil litter layer, soil mineral layer, subsoil, snow, streams, and lakes. Dominant physiological processes carried out by biota include photosynthesis, grazing, decomposition, respiration, nitrogen fixation, ammonification, and nitrification. Key abiotic processes include insolation (sunlight), transport, precipitation, runoff, infiltration, dissolution, and acid/base and oxidation/reduction reactions (see Table 1.4). Net budgets can be constructed for ecosystems; when inputs match outputs, the systems are said to be “steady state”. 9781405136471_4_001.qxd 1/15/08 9:21 Page 10
11CHAPTERISIGNIFICANCE,HISTORY,AND CHALLENGESOFENVIRONMENTALMICROBIOLOGYTable 1.4Types of biogeochemical processes thattypically occur and interact in real-world habitatsTypeProcessesPhysicalInsolation (sunlight),atmosphericprecipitation,waterinfiltration,waterevaporation,transporterosion,runoff,dilution,advection,dispersion,volatilization,sorptionChemicalDissolution of mineralsandorganic compounds,precipitation,formation of secondaryminerals,photolysis,acid/basereactions,reactions catalyzed by clay-mineral surfaces,reduction,oxidation,organicequilibria,inorganicequilibriaBiologicalGrowth,death, excretion,differentiation,foodwebs,grazing,migration,predationcompetition,parasitism, symbiosis,decompositionof high molecular weightbiopolymersto lowmolecular weightmonomers,respiration,photosynthesis,nitrogenfixation,nitrification,denitrification,ammonification,sulfatereduction,sulfur oxidation,ironoxidation/reduction,manganeseoxidation/reduction,anaerobicoxidationofmethane,anaerobicoxidation ofammonia,acetogenesis,methanogenesisinfluencefluxesof materials into,outof,andwithinthesystemarealsodynamic.Atthescale of ~1 m,humansareableto surveyhabitats and maptheoccurrence of both abiotic (rocks, soils,gasses,water)and biotic(plants,animals)componentsofthewatershed.Atthisscale,muchprogresshasbeenmadetowardunderstandingecosystems.Biogeochemicalecosystemecologists havegained far-reaching insights into how such systems workby performing a variety of measurements in basins whose sealed bedrockfoundations allow ecosystem budgets to be constructed (Figure 1.3).When integrated over time and space, the chemical constituents (water,carbon,nitrogen,sulfur,etc.)measured in incomingprecipitation,inoutflowing waters, and in storage reservoirs (lakes, soil, the biota) canprovide a rigorous basis for understanding how watersheds work and howthey respond toperturbations (Likens and Bormann,1995).Understand-ing watershed (as well as global)biogeochemical cycles relies upon rig-orous data sets and well-defined physical and conceptual boundaries.Fora given system,regardless of its size, if it is in steadystate, the inputsmust equal the outputs (Figure 1.3).By the same token, if input andoutputtermsforagivensystemarenotinbalance,keybiogeochemicalparameters of interest may be changing with time.Net loss or gain is depend-entonrelativeratesofconsumptionandproduction.Biogeochemicaldatasets provide a means for answering crucial ecological questions such as:Isthesystem in steadystate?Are carbon and nitrogen accruing ordiminishing?Does input of atmosphericpollutantsimpact ecosystemfunction?Whatgoodsandservicesdointactwatershedsprovideintermsof water and soil quality? More details on measuring and modeling bio-geochemical cycles arepresented in Chapter7
Table 1.4 Types of biogeochemical processes that typically occur and interact in real-world habitats Type Processes Physical Insolation (sunlight), atmospheric precipitation, water infiltration, water evaporation, transport, erosion, runoff, dilution, advection, dispersion, volatilization, sorption Chemical Dissolution of minerals and organic compounds, precipitation, formation of secondary minerals, photolysis, acid/base reactions, reactions catalyzed by clay-mineral surfaces, reduction, oxidation, organic equilibria, inorganic equilibria Biological Growth, death, excretion, differentiation, food webs, grazing, migration, predation, competition, parasitism, symbiosis, decomposition of high molecular weight biopolymers to low molecular weight monomers, respiration, photosynthesis, nitrogen fixation, nitrification, denitrification, ammonification, sulfate reduction, sulfur oxidation, iron oxidation/reduction, manganese oxidation/reduction, anaerobic oxidation of methane, anaerobic oxidation of ammonia, acetogenesis, methanogenesis influence fluxes of materials into, out of, and within the system are also dynamic. At the scale of ~1 m, humans are able to survey habitats and map the occurrence of both abiotic (rocks, soils, gasses, water) and biotic (plants, animals) components of the watershed. At this scale, much progress has been made toward understanding ecosystems. Biogeochemical ecosystem ecologists have gained far-reaching insights into how such systems work by performing a variety of measurements in basins whose sealed bedrock foundations allow ecosystem budgets to be constructed (Figure 1.3). When integrated over time and space, the chemical constituents (water, carbon, nitrogen, sulfur, etc.) measured in incoming precipitation, in outflowing waters, and in storage reservoirs (lakes, soil, the biota) can provide a rigorous basis for understanding how watersheds work and how they respond to perturbations (Likens and Bormann, 1995). Understanding watershed (as well as global) biogeochemical cycles relies upon rigorous data sets and well-defined physical and conceptual boundaries. For a given system, regardless of its size, if it is in steady state, the inputs must equal the outputs (Figure 1.3). By the same token, if input and output terms for a given system are not in balance, key biogeochemical parameters of interest may be changing with time. Net loss or gain is dependent on relative rates of consumption and production. Biogeochemical data sets provide a means for answering crucial ecological questions such as: Is the system in steady state? Are carbon and nitrogen accruing or diminishing? Does input of atmospheric pollutants impact ecosystem function? What goods and services do intact watersheds provide in terms of water and soil quality? More details on measuring and modeling biogeochemical cycles are presented in Chapter 7. CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 11 9781405136471_4_001.qxd 1/15/08 9:21 Page 11
12CHAPTERISIGNIFICANCE,HISTORY,AND CHALLENGESOFENVIRONMENTALMICROBIOLOGYLarge-scale watershed data capture net changes in complex, open sys-tems.Thoughprofoundandinsightful,thisapproachleavesmechanisticmicroscale cause-and-effect linkages unaddressed. Measures of netchange do not addressdynamic controls on rates of processes thatgen-erate(versusthosethatconsume)componentsofagivennutrientpool.Indeed, the intricate microscale interactions between biotic and abioticfield processes are often masked in data gathered in large-scale systems.Thus,ecosystem-level biogeochemical data may often fail to satisfy thescientific needfor details of theprocesses of interest.An example of stepstowardamechanisticunderstandingofecosystemprocessisshowninFigure1.4.This model shows a partial synthesis of ecosystem processes thatgovern the fate of nitrogen in a watershed. Inputs, flows, nutrient pools,biological players,physiological reactions,and transport processes aredepicted. Understanding and measuring the sizes of nitrogenous pools,theirtransformations,rates,fluxes,andtheactivebioticagentsrepresentsa major challenge for both biogeochemists and microbiologists.YetFigure 1.4 considerably simplifies the processes that actually occur in real-world watersheds because many details are missing and comparablycomplexreactions and interactions apply simultaneously to other nutri-ent elements (C, S, P, O, H, etc.). Consider a data set in which concen-trations of ammonium (akeyform of nitrogen)are found to fluctuate instream sediments.Interpreting such field measurements is very difficultbecause the ammonium pool at anygiven moment is controlled byprocesses of production (e.g.,ammonificationbymicroorganisms),con-sumption (e.g.,aerobicandanaerobicammonia-oxidizingmicroorganisms,nutrient uptake by all organisms) and transport (e.g.,entrainment inflowing water, diffusion, dilution, physical disturbance of sediment).Clearly,the many compounded intricacies of nutrientcycling and trophicandbiochemical interactions in a field habitatmakebiogeochem-ical processes,especially those catalyzedbymicroorganisms,difficulttodecipher.I.5MANYDISCIPLINESANDTHEIRINTEGRATIONGiven the complexity of real-world habitats that are home to microorganisms(see above),what is to be done?.How can we contend with complexity?Whatapproaches can productivelyyield clear information thatenhances our under-standing of the role of microorganisms in maintaining our world?How do microorganisms carry out specific transformations on specific com-pounds in soils, sediments,and waters?Answer:The optimisticanswertothese questions is simple:We usethe many tools on handto Iwenty-first century science
Large-scale watershed data capture net changes in complex, open systems. Though profound and insightful, this approach leaves mechanistic microscale cause-and-effect linkages unaddressed. Measures of net change do not address dynamic controls on rates of processes that generate (versus those that consume) components of a given nutrient pool. Indeed, the intricate microscale interactions between biotic and abiotic field processes are often masked in data gathered in large-scale systems. Thus, ecosystem-level biogeochemical data may often fail to satisfy the scientific need for details of the processes of interest. An example of steps toward a mechanistic understanding of ecosystem process is shown in Figure 1.4. This model shows a partial synthesis of ecosystem processes that govern the fate of nitrogen in a watershed. Inputs, flows, nutrient pools, biological players, physiological reactions, and transport processes are depicted. Understanding and measuring the sizes of nitrogenous pools, their transformations, rates, fluxes, and the active biotic agents represents a major challenge for both biogeochemists and microbiologists. Yet Figure 1.4 considerably simplifies the processes that actually occur in realworld watersheds because many details are missing and comparably complex reactions and interactions apply simultaneously to other nutrient elements (C, S, P, O, H, etc.). Consider a data set in which concentrations of ammonium (a key form of nitrogen) are found to fluctuate in stream sediments. Interpreting such field measurements is very difficult because the ammonium pool at any given moment is controlled by processes of production (e.g., ammonification by microorganisms), consumption (e.g., aerobic and anaerobic ammonia-oxidizing microorganisms, nutrient uptake by all organisms) and transport (e.g., entrainment in flowing water, diffusion, dilution, physical disturbance of sediment). Clearly, the many compounded intricacies of nutrient cycling and trophic and biochemical interactions in a field habitat make biogeochemical processes, especially those catalyzed by microorganisms, difficult to decipher. 1.5 MANY DISCIPLINES AND THEIR INTEGRATION 12 CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY • Given the complexity of real-world habitats that are home to microorganisms (see above), what is to be done? • How can we contend with complexity? • What approaches can productively yield clear information that enhances our understanding of the role of microorganisms in maintaining our world? • How do microorganisms carry out specific transformations on specific compounds in soils, sediments, and waters? Answer: The optimistic answer to these questions is simple: We use the many tools on hand to twenty-first century science. 9781405136471_4_001.qxd 1/15/08 9:21 Page 12
13CHAPTERISIGNIFICANCE,HISTORY,AND CHALLENGESOFENVIRONMENTAL MICROBIOLOGYMICROBIALECOSYSTEMOXIDATIONREDUCTIONECOSYSTEMINPUTSSTORAGESPROCESSESOUTPUTSPlant organic NMicrobiologicalroroeNfixationInvertebrate andvertebrategrazersand predatorsNH,VolatilizationARun offMicroorganismsNOOrganic NSoil organic NPlant harvest(manure waste)naNO;LeachingInorganicSoil soluble andfertilizersexchangeable N(NH. NO)oeaNO2N in dry andwet depositionClay-fixed N(NH)Nz, N,OGaseous lossesFigure1.4 Flowmodel ofnitrogen (N)cyclinginterrestrialecosystems.Shownarebasicinputs,storages,microbial processes,outputs,andbothbioticandabioticinteractions.(Reprintedandmodified withpermissionfromMadsen,E.L.1998.Epistemologyof environmental microbiology.Environ.Sci.Technol.32:429-439.Copyright1998,American ChemicalSociety.)The principles are sound, the insights are broad, and the sophisticatedtechnologiesareeverexpanding.Tocounterbalancethechallengesofeco-system complexity,we can utilize:(i)robust,predictablerules of chemicalthermodynamics,geochemical reactions,physiology,andbiochemistry:(i)measurementtechniquesfromanalytical chemistry,hydrogeology,physi-ology,microbiology,molecularbiology;and(ii)compound-specificprop-erties such as solubility,volatility,toxicity,and susceptibilitytobiotic andabiotic reactions.A partial listing of the many areas of science that con-tribute to advancements in environmental microbiology.with accom-panying synopses and references, appears in Table 1.5.Conceptually,environmental microbiology resides at the interfacebetween two vigorouslyexpandingdisciplines:environmental scienceand
CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 13 Organic N (manure waste) Invertebrate and vertebrate grazers and predators Microorganisms NH4 + NO2 – NO2 – N2, N2O NO3 – Volatilization Ammonification Nitrification Denitrification Run off Plant harvest Leaching Gaseous losses Plant organic N Soil organic N Soil soluble and exchangeable N Clay-fixed N (NH4 + ) N in dry and wet deposition Inorganic fertilizers (NH4 + , NO3 – ) Microbiological N fixation ECOSYSTEM INPUTS STORAGES MICROBIAL OXIDATION REDUCTION PROCESSES ECOSYSTEM OUTPUTS Figure 1.4 Flow model of nitrogen (N) cycling in terrestrial ecosystems. Shown are basic inputs, storages, microbial processes, outputs, and both biotic and abiotic interactions. (Reprinted and modified with permission from Madsen, E.L. 1998. Epistemology of environmental microbiology. Environ. Sci. Technol. 32:429–439. Copyright 1998, American Chemical Society.) The principles are sound, the insights are broad, and the sophisticated technologies are ever expanding. To counterbalance the challenges of ecosystem complexity, we can utilize: (i) robust, predictable rules of chemical thermodynamics, geochemical reactions, physiology, and biochemistry; (ii) measurement techniques from analytical chemistry, hydrogeology, physiology, microbiology, molecular biology; and (iii) compound-specific properties such as solubility, volatility, toxicity, and susceptibility to biotic and abiotic reactions. A partial listing of the many areas of science that contribute to advancements in environmental microbiology, with accompanying synopses and references, appears in Table 1.5. Conceptually, environmental microbiology resides at the interface between two vigorously expanding disciplines: environmental science and 9781405136471_4_001.qxd 1/15/08 9:21 Page 13
Table 1.5Disciplines that contributeto environmental microbiologySubject matter and contribution toReferencesDisciplineEnvironmental MicrobiologyEnvironmentalThe study of microorganisms that inhabit the EarthMaier et al., 2000;Rochelle, 2001:microbiologyand their roles in carrying out processes in bothnatural and human-made systems, emphasis isSpencer and Ragouton interfaces between environmental sciencesdeSpencer,2004and microbial diversityAtlas and Bartha,Microbial ecologyThe study of interrelationships between1998; Burlage et al.,microorganismsandtheirbioticandabioticsurroundings1998;StaleyandReysenbach,2002;Osborn,2003:McArthur,2006Soil microbiologyEnvironmental microbiology andmicrobial ecologyvan Elsas et al.,1997:Huang et al.,2002;of the soil habitat;with emphasis on nutrientSylvia et al., 2005cycling,plantand animal life,and terrestrialecosystemsEnvironmental microbiologyandmicrobial ecologyFord, 1993;Bitton,Aquaticmicrobiologyofaquatichabitats(oceans,lakes,streams)1999;Kirchman,2000groundwaters)MicrobiologyHolistic study of the function of microbial cells andMadigan and Martinko,their impact on medicine,industry,environment,2006;Schaechteretal.,2006and technologyMicrobial physiologyIntegrated mechanistic examination of bacteriallyGottschalk,1986;White,1995;mediated processes,especiallygrowth andLengeler et al., 1999metabolismMicroscopyTheuseofoptics, lenses, microscopes,imagingMurphy.2001devices,and imageanalysissystemsto visualizesmall structuresBiochemistryMolecular examination of the structure andDevlin, 2001;Nichollsfunction of subcellular processes, especially ATPand Ferguson, 2002;generation,organelles,biopolymers,enzymesNelsonand Cox,2005and membranesBiotechnologyThe integrated use of biochemistry,molecular,Glick and Pasternack,biology,genetics,microbiology.plant and animal2003science,and chemical engineering to achieveindustrialgoodsand servicesSchlesinger, 1997;BiogeochemistySystems approach to the chemical reactionsbetween biological,geological,andatmosphericFenchel et al., 1998components of the EarthSnyderandMicrobial geneticsMolecular mechanistic basis of heredity,evolution,Champness,2003mutation inprokaryotes,and theirbiotechnological applicationOmicsBaxevanis andUmbrella term that encompasses bioinfomatics-Ouellette,2001;basedsystematicanalysisofgenes (genomics),Sensen, 2002proteins (proteomics),mRNA (transcriptomics)Twyman,2004;metabolites (metabolomics).etc.Zhou et al., 2004
Table 1.5 Disciplines that contribute to environmental microbiology Discipline Environmental microbiology Microbial ecology Soil microbiology Aquatic microbiology Microbiology Microbial physiology Microscopy Biochemistry Biotechnology Biogeochemisty Microbial genetics Omics Subject matter and contribution to Environmental Microbiology The study of microorganisms that inhabit the Earth and their roles in carrying out processes in both natural and human-made systems; emphasis is on interfaces between environmental sciences and microbial diversity The study of interrelationships between microorganisms and their biotic and abiotic surroundings Environmental microbiology and microbial ecology of the soil habitat; with emphasis on nutrient cycling, plant and animal life, and terrestrial ecosystems Environmental microbiology and microbial ecology of aquatic habitats (oceans, lakes, streams, groundwaters) Holistic study of the function of microbial cells and their impact on medicine, industry, environment, and technology Integrated mechanistic examination of bacterially mediated processes, especially growth and metabolism The use of optics, lenses, microscopes, imaging devices, and image analysis systems to visualize small structures Molecular examination of the structure and function of subcellular processes, especially ATP generation, organelles, biopolymers, enzymes, and membranes The integrated use of biochemistry, molecular, biology, genetics, microbiology, plant and animal science, and chemical engineering to achieve industrial goods and services Systems approach to the chemical reactions between biological, geological, and atmospheric components of the Earth Molecular mechanistic basis of heredity, evolution, mutation in prokaryotes, and their biotechnological application Umbrella term that encompasses bioinfomaticsbased systematic analysis of genes (genomics), proteins (proteomics), mRNA (transcriptomics), metabolites (metabolomics), etc. References Maier et al., 2000; Rochelle, 2001; Spencer and Ragout de Spencer, 2004 Atlas and Bartha, 1998; Burlage et al., 1998; Staley and Reysenbach, 2002; Osborn, 2003; McArthur, 2006 van Elsas et al., 1997; Huang et al., 2002; Sylvia et al., 2005 Ford, 1993; Bitton, 1999; Kirchman, 2000 Madigan and Martinko, 2006; Schaechter et al., 2006 Gottschalk, 1986; White, 1995; Lengeler et al., 1999 Murphy, 2001 Devlin, 2001; Nicholls and Ferguson, 2002; Nelson and Cox, 2005 Glick and Pasternack, 2003 Schlesinger, 1997; Fenchel et al., 1998 Snyder and Champness, 2003 Baxevanis and Ouellette, 2001; Sensen, 2002; Twyman, 2004; Zhou et al., 2004 9781405136471_4_001.qxd 1/15/08 9:21 Page 14