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CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 5 Nitrogen Sulfur Other elements Fw, freshwater; FwS, freshwater sediment; Gw, groundwater; Os, ocean sediments; Ow, ocean waters; Sl, soil; Sw, sewage. Nitrogen fixation Ammonium oxidation Anaerobic ammonium oxidation Denitrification Sulfur oxidation Sulfate reduction Hydrogen oxidation Mercury methylation and reduction (Per)chlorate reduction Uranium reduction Arsenate reduction Iron oxidation, acid mine drainage N2 gas becomes ammonia Ammonia becomes nitrite and nitrate Nitrite and ammonia become N2 gas Nitrate is used as an electron acceptor and converted to N2 gas Sulfide and sulfur become sulfate Sulfate is used as an electron acceptor and converted to sulfur and sulfide Hydrogen is oxidized to H+ , electrons reduce other substances Organic mercury is formed and mercury ion is converted to metallic mercury Oxidants in rocket fuel and other sources are converted to chloride Uranium oxyanion is used as an electron acceptor; hence immobilized Arsenic oxyanion is used as an electron acceptor; hence toxicity is diminished Iron sulfide ores are oxidized, strong acidity is generated Ow, Sl Sl, Sw Os, Sw Sl, Sw Os Os Sl, Os, Sw, FwS, Os Gw Gw FwS, Gw FwS, Gw Karl et al., 2002 Stark and Hart, 1997; Kowalchuk and Stephen, 2001 Dalsgaard et al., 2003; van Niftrik et al., 2004 Zumft, 1997; van Breemen et al., 2002 Taylor and Wirsen, 1997 Habicht and Canfield, 1996 Schink, 1997 Morel et al., 1998; Sigel et al., 2005 Coates and Achenbach, 2004 Lovley, 2003 Oremland and Stolz, 2003 Edwards et al., 2000 9781405136471_4_001.qxd 1/15/08 9:21 Page 5
6CHAPTERISIGNIFICANCE,HISTORY,ANDCHALLENGESOFENVIRONMENTALMICROBIOLOGYa sampling oftheecological and biogeochemical processesthatmicroor-ganisms catalyze in aquatic or terrestrial habitats. Additional details of biogeochemical processes and ways to recognize and understand them arepresented in Chapters 3and7.I.3ABRIEFHISTORYOFENVIRONMENTALMICROBIOLOGYEarlyfoundationsof microbiologyrestwithmicroscopicobservationsoffungalsporulation(byRobertHookeinl665)and"weeanimalcules"-truebacterialstructures(byAntonievanLeeuwenhoekin1684).Inthelatterhalfofthenineteenthcentury,FerdinandCohn,LouisPasteur,andRobertKoch wereresponsiblefor methodological innovations in aseptictechnique and isolation of microorganisms (Madigan and Martinko,2o06).These,inturn,allowedmajoradvancespertinenttospontaneousgeneration, disease causation, and germ theory.Environmental microbiologyalso experienced major advancements inthe nineteenth century: these extend through to the present. Environ-mental microbiology'sroots spanmany continentsand countries (Russia,Japan,Europe, and England) and a complex tapestry of contributionshas developed.To a large degree,the challenges and discoveries in envir-onmental microbiology have been habitat-specific.Thus,one approachfor grasping thehistory and traditions of environmental microbiologyis to recognize subdisciplines such as marine microbiology,soil micro-biology,rumenmicrobiology,sedimentmicrobiology.geomicrobiology,andsubsurface microbiology.In addition, the contributions from variouscenters of training can also sometimes be easilydiscerned.These neces-sarily revolved around various investigators and the institutions wheretheywere based.As early as 1838 in Germany, C. G. Ehrenberg was developing the-ories about the influence of thebacterium,Gallionella ferruginea, on thegeneration of iron deposits inbogs(Ehrlich,2002).Furthermore,earlyforays intomarine microbiology byA.Certes (in 1882),H.L.Russell, P.Regnard, B.Fischer, and P.and G. C. Frankland allowed the completionof preliminary surveys ofmicroorganisms from far-ranging oceanicwaters and sediments (Litchfield, 1976).At theUniversityof Delft (the Netherlands)near the end of the nine-teenth century,M.W.Beijerinck (Figure 1.1)founded the Delft Schooltraditions of elective enrichment techniques (see Section 6.2)thatallowed Beijerinck's crucial discoveries including microbiological trans-formations of nitrogenand carbon,andalso otherelements suchas man-ganese(vanNiel,1967AtlasandBartha,1998;MadiganandMartinko,2006).Thehelm of theDelftSchoolchangedhandsfromBeijerincktoA. J. Kluyver, and the traditions have been continued in the Nether-lands,Germany,andotherpartsof Europethroughtothepresent.After
a sampling of the ecological and biogeochemical processes that microorganisms catalyze in aquatic or terrestrial habitats. Additional details of biogeochemical processes and ways to recognize and understand them are presented in Chapters 3 and 7. 1.3 A BRIEF HISTORY OF ENVIRONMENTAL MICROBIOLOGY Early foundations of microbiology rest with microscopic observations of fungal sporulation (by Robert Hooke in 1665) and “wee animalcules” – true bacterial structures (by Antonie van Leeuwenhoek in 1684). In the latter half of the nineteenth century, Ferdinand Cohn, Louis Pasteur, and Robert Koch were responsible for methodological innovations in aseptic technique and isolation of microorganisms (Madigan and Martinko, 2006). These, in turn, allowed major advances pertinent to spontaneous generation, disease causation, and germ theory. Environmental microbiology also experienced major advancements in the nineteenth century; these extend through to the present. Environmental microbiology’s roots span many continents and countries (Russia, Japan, Europe, and England) and a complex tapestry of contributions has developed. To a large degree, the challenges and discoveries in environmental microbiology have been habitat-specific. Thus, one approach for grasping the history and traditions of environmental microbiology is to recognize subdisciplines such as marine microbiology, soil microbiology, rumen microbiology, sediment microbiology, geomicrobiology, and subsurface microbiology. In addition, the contributions from various centers of training can also sometimes be easily discerned. These necessarily revolved around various investigators and the institutions where they were based. As early as 1838 in Germany, C. G. Ehrenberg was developing theories about the influence of the bacterium, Gallionella ferruginea, on the generation of iron deposits in bogs (Ehrlich, 2002). Furthermore, early forays into marine microbiology by A. Certes (in 1882), H. L. Russell, P. Regnard, B. Fischer, and P. and G. C. Frankland allowed the completion of preliminary surveys of microorganisms from far-ranging oceanic waters and sediments (Litchfield, 1976). At the University of Delft (the Netherlands) near the end of the nineteenth century, M. W. Beijerinck (Figure 1.1) founded the Delft School traditions of elective enrichment techniques (see Section 6.2) that allowed Beijerinck’s crucial discoveries including microbiological transformations of nitrogen and carbon, and also other elements such as manganese (van Niel, 1967; Atlas and Bartha, 1998; Madigan and Martinko, 2006). The helm of the Delft School changed hands from Beijerinck to A. J. Kluyver, and the traditions have been continued in the Netherlands, Germany, and other parts of Europe through to the present. After 6 CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 9781405136471_4_001.qxd 1/15/08 9:21 Page 6
CHAPTERISIGNIFICANCE,HISTORY,AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGytraininginDelft with Beijerinck andKluyver, C. B. van Niel was asked byL.G.M.Baas Becking to establisheda research program at Stanford Uni-versity'sHopkinsMarineStation(done in 1929), where R. Y. Stainer,R.Hungate,M.Doudoroff and manyothers were trained, later establishingtheir own research programs at otherinstitutions in the United States (vanNiel, 1967),S. Winogradsky (Figure 1.2) is re-garded bymany asthefounder of soilmicrobiology (Atlas and Bartha, 1998).Working in the latter part of the nine-teenth and early decades of the twen-tieth centuries,Winogradsky's careercontributed immensely to our know-ledgeofsoilandenvironmentalmicro-biology,especially regarding microbialmetabolism of sulfur,iron,nitrogen,and manganese.In1949,much ofWinogradsky'sworkwaspublishedasa major treatise entitled, Microbiologiedu sol, problemes et methods: cinquanteans de recherches. Oeuvres Completes(Winogradsky,1949).Manyof themarinemicrobiologistsBeyergkin the early twentieth century focusedtheir attention on photoluminescentbacteria (E. Pluger, E. W.Harvey.H.Figure 1.1 Martinus Beijerinck (1851-1931).FounderMolisch,W.Beneche,G.H.Drew,andof theDelft School of Microbiology,M.BeijerinckJ.W.Hastings).Later,transformationworked until the age of 7o at the University of Delft,by marine microorganisms of carbonthe Netherlands. He made major discoveries in electiveand nitrogen were explored, as well asenrichment techniques and used them to advance theadaptationlo low-temperaturehab-understandingofhowmicroorganismstransformitats (S.A. Waksman, C.E.ZoBell, S.nitrogen, sulfur, and other elements. (ReproducedJ.Niskin, O.Holm-Hansen, and N. V.withpermissionfromtheAmericanSocietyforand V.S.Butkevich).The mid-twen-Microbiology Archives, USA.)tieth century marine studies continuedexploration ofthephysiologicaland structural responses ofmicroorgan-isms to salt,low temperature,and pressure (J.M. Shewan,H.W.Jannasch, R.Y.Morita, R.R. Colwell, E. Wada, A. Hattori, and N.Taga).Also,studies of nutrientuptake (J.E.Hobbie)and food chains consti-tuting the"microbial loop"were conducted (L.R.Pomeroy)
training in Delft with Beijerinck and Kluyver, C. B. van Niel was asked by L. G. M. Baas Becking to established a research program at Stanford University’s Hopkins Marine Station (done in 1929), where R. Y. Stainer, R. Hungate, M. Doudoroff and many others were trained, later establishing their own research programs at other institutions in the United States (van Niel, 1967). S. Winogradsky (Figure 1.2) is regarded by many as the founder of soil microbiology (Atlas and Bartha, 1998). Working in the latter part of the nineteenth and early decades of the twentieth centuries, Winogradsky’s career contributed immensely to our knowledge of soil and environmental microbiology, especially regarding microbial metabolism of sulfur, iron, nitrogen, and manganese. In 1949, much of Winogradsky’s work was published as a major treatise entitled, Microbiologie du sol, problémes et methods: cinquante ans de recherches. Oeuvres Complétes (Winogradsky, 1949). Many of the marine microbiologists in the early twentieth century focused their attention on photoluminescent bacteria (E. Pluger, E. W. Harvey, H. Molisch, W. Beneche, G. H. Drew, and J. W. Hastings). Later, transformation by marine microorganisms of carbon and nitrogen were explored, as well as adaptation to low-temperature habitats (S. A. Waksman, C. E. ZoBell, S. J. Niskin, O. Holm-Hansen, and N. V. and V. S. Butkevich). The mid-twentieth century marine studies continued exploration of the physiological and structural responses of microorganisms to salt, low temperature, and pressure (J. M. Shewan, H. W. Jannasch, R. Y. Morita, R. R. Colwell, E. Wada, A. Hattori, and N. Taga). Also, studies of nutrient uptake (J. E. Hobbie) and food chains constituting the “microbial loop” were conducted (L. R. Pomeroy). CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 7 Figure 1.1 Martinus Beijerinck (1851–1931). Founder of the Delft School of Microbiology, M. Beijerinck worked until the age of 70 at the University of Delft, the Netherlands. He made major discoveries in elective enrichment techniques and used them to advance the understanding of how microorganisms transform nitrogen, sulfur, and other elements. (Reproduced with permission from the American Society for Microbiology Archives, USA.) 9781405136471_4_001.qxd 1/15/08 9:21 Page 7
8CHAPTERISIGNIFICANCE,HISTORY,AND CHALLENGESOFENVIRONMENTALMICROBIOLOGYAt Rutgers University.Selman A.Waksman was perhaps the foremostAmericanscholarinthedisciplineof soilmicrobiologyMany of the Rutgerstraditions in soil microbiology wereinitiated by J.Lipman,Waksman's pre-decessor (R.Bartha,personal commun-ication;Waksman,1952).Waksmanproducednumeroustreatisesthatsummarized the historystatus,andfrontiers of soil microbiology,often incollaboration with R. Starkey.AmongtheprominentworkspublishedbyWaksman are"Soil microbiology in1924:anattemptatan analysisandasynthesis"(Waksman,1925),Principlesof Soil Microbiology(Waksman,1927),"Soil microbiology as a field of sci-ence"(Waksman,1945),andSoilMicro-biology (Waksman,1952).Asteady flowof Rutgers-based contributions to en-vironmental microbiology continue tobepublished (e.g,Youngand Cerniglia,1995;Haggblom andBossert,2003)Inthe1920sand1930s.E.B.Fredand collaborators,I.L.Baldwin and EMcCoy,comprised a unique cluster ofinvestigators whose interests focusedineroulnon theRhizobium-legume symbiosis.Several decades later at the UniversityofWisconsin,T.D.Brockandhisstu-Figure1.2SergeiWinogradsky(1856-1953).Amajordentsmadeimportantcontributionstocontributor toknowledge of soil microbiology,S.microbial ecology,thermophily.andWinogradsydescribedmicrobialcyclingof sulfurandgeneral microbiology. Another gra-nitrogen compounds.Hedeveloped the"Winogradskyduate of the University of Wisconsin,columnforgrowingdiversephysiologicaltypes ofH.L.Ehrlich earned a Ph.D.in 1951aerobicand anaerobic,heterotrophicand photosyntheticand,after movingtoRensselaerbacteria across gradients of oxygen, sulfur, and light.PolytechnicInstitute,carried outstud-(Reproduced with permission from the Smith Collegeieson thebacteriology of manganeseArchives,SmithCollege.)nodules, among other topics.Author offourcomprehensiveeditions of Geomicrobiology,H.L.Ehrlich is,formany,the founder of this discipline.Another University of Wisconsin graduate,M.Alexander,moved toCornellUniversityin1955.ForfourdecadespriortoAlexander'sarrivalsoilmicrobiological researchwasconductedat CornellbyJ.K.WilsonandF.Broadbent.From1955tothepresent,Alexander'scontributions
At Rutgers University, Selman A. Waksman was perhaps the foremost American scholar in the discipline of soil microbiology. Many of the Rutgers traditions in soil microbiology were initiated by J. Lipman, Waksman’s predecessor (R. Bartha, personal communication; Waksman, 1952). Waksman produced numerous treatises that summarized the history, status, and frontiers of soil microbiology, often in collaboration with R. Starkey. Among the prominent works published by Waksman are “Soil microbiology in 1924: an attempt at an analysis and a synthesis” (Waksman, 1925), Principles of Soil Microbiology (Waksman, 1927), “Soil microbiology as a field of science” (Waksman, 1945), and Soil Microbiology (Waksman, 1952). A steady flow of Rutgers-based contributions to environmental microbiology continue to be published (e.g., Young and Cerniglia, 1995; Haggblom and Bossert, 2003). In the 1920s and 1930s, E. B. Fred and collaborators, I. L. Baldwin and E. McCoy, comprised a unique cluster of investigators whose interests focused on the Rhizobium–legume symbiosis. Several decades later at the University of Wisconsin, T. D. Brock and his students made important contributions to microbial ecology, thermophily, and general microbiology. Another graduate of the University of Wisconsin, H. L. Ehrlich earned a Ph.D. in 1951 and, after moving to Rensselaer Polytechnic Institute, carried out studies on the bacteriology of manganese nodules, among other topics. Author of four comprehensive editions of Geomicrobiology, H. L. Ehrlich is, for many, the founder of this discipline. Another University of Wisconsin graduate, M. Alexander, moved to Cornell University in 1955. For four decades prior to Alexander’s arrival, soil microbiological research was conducted at Cornell by J. K. Wilson and F. Broadbent. From 1955 to the present, Alexander’s contributions 8 CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY Figure 1.2 Sergei Winogradsky (1856–1953). A major contributor to knowledge of soil microbiology, S. Winogradsy described microbial cycling of sulfur and nitrogen compounds. He developed the “Winogradsky column” for growing diverse physiological types of aerobic and anaerobic, heterotrophic and photosynthetic bacteria across gradients of oxygen, sulfur, and light. (Reproduced with permission from the Smith College Archives, Smith College.) 9781405136471_4_001.qxd 1/15/08 9:21 Page 8
9CHAPTERISIGNIFICANCE,HISTORY,AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGyto soil microbiologyhaveexaminedabroad diversity of phenomena,whichincludevarious transformations of nitrogen,predator-prey relations,microbialmetabolismofpesticidesandenvironmentalpollutants,andadvancementsinenvironmentaltoxicology.Manyenvironmentalmicro-biologists havereceived trainingwith M.Alexander and becomeprom-inent investigators,including J.M.Tiedje.Other schools and individuals in Britain,Italy,France,Belgium and otherparts ofEurope,Japan,Russiaand other parts of Asia,Africa,Australia,the United States and other parts of the Americas certainly have con-tributed in significant ways to advancementsin environmentalmicro-biology.An insightful reviewof the history of soil microbiology.withspecial emphasis on eastern European and Russian developments waswrittenbyMacura(1974).Themanyhistorical milestones inthedevelopment of environmentalmicrobiology(most of whicharesharedwithbroaderfields of biologyand microbiology)have been reviewed by Atlas and Bartha (1998),Brock(1961),LechevalierandSolotorovsky(1965).Macura(1974)MadiganandMartinko(2006),vanNiel(1967),Waksman(1925,19271952),and others. Some of the highlights are listed in Table 1.3.Table 1.3Selected landmark events in the historyof environmental microbiologyThefirst visualization of microscopic lifebyvan Leeuwenhoek in 1684The role ofmicroorganisms as causativeagents of fermentations discovered by Pasteur in 1857Theuseofgelatinplatesforenumerationof soilmicroorganismsbyKochin1881-Nitrogen fixation by nodules on the roots of legumes discovered by Hellriegel and Wilfarth in1885The use of elective enrichmentmethods,byBeijerinck and Winogradsky,in the isolation of singleorganismsabletocarryoutammonification,nitrification,andbothsymbioticandnonsymbioticnitrogen fixationRecognition of thediverse populations in soil (e-g.,bacteria,fungi,algae,protozoa,nematodes,insectlarvae)-Documentation ofanaerobiccellulosedecompositionbyOmelianski in1902The study of sulfur-utilizing phototrophicbacteriaby vanNiel and othersThe specificity of legume-nodulatingbacteria (Fred etal..1932)-Thediscoveryand developmentofantibiotics-Direct microscopic methods of examining environmental microorganisms via staining and contact-slideproceduresThedevelopment of radiotracertechniquesA diversity of advancements in analytical chemistry for detecting and quantifying biochemicallyand environmentallyrelevantcompoundsDevelopments inmolecularphylogeny (Woese,1987,1992;Pace,1997)Theapplicationofmolecularmethodsto environmental microbiology(Olsenetal.,1986;Paceetal.,1986;Amann etal.,1991,1995:Ward etal.,1993;White,1994;van Elsas etal.,1997:MadiganandMartinko,2006)
to soil microbiology have examined a broad diversity of phenomena, which include various transformations of nitrogen, predator–prey relations, microbial metabolism of pesticides and environmental pollutants, and advancements in environmental toxicology. Many environmental microbiologists have received training with M. Alexander and become prominent investigators, including J. M. Tiedje. Other schools and individuals in Britain, Italy, France, Belgium and other parts of Europe, Japan, Russia and other parts of Asia, Africa, Australia, the United States and other parts of the Americas certainly have contributed in significant ways to advancements in environmental microbiology. An insightful review of the history of soil microbiology, with special emphasis on eastern European and Russian developments was written by Macura (1974). The many historical milestones in the development of environmental microbiology (most of which are shared with broader fields of biology and microbiology) have been reviewed by Atlas and Bartha (1998), Brock (1961), Lechevalier and Solotorovsky (1965), Macura (1974), Madigan and Martinko (2006), van Niel (1967), Waksman (1925, 1927, 1952), and others. Some of the highlights are listed in Table 1.3. CHAPTER I SIGNIFICANCE, HISTORY, AND CHALLENGES OF ENVIRONMENTAL MICROBIOLOGY 9 Table 1.3 Selected landmark events in the history of environmental microbiology • The first visualization of microscopic life by van Leeuwenhoek in 1684 • The role of microorganisms as causative agents of fermentations discovered by Pasteur in 1857 • The use of gelatin plates for enumeration of soil microorganisms by Koch in 1881 • Nitrogen fixation by nodules on the roots of legumes discovered by Hellriegel and Wilfarth in 1885 • The use of elective enrichment methods, by Beijerinck and Winogradsky, in the isolation of single organisms able to carry out ammonification, nitrification, and both symbiotic and nonsymbiotic nitrogen fixation • Recognition of the diverse populations in soil (e.g., bacteria, fungi, algae, protozoa, nematodes, insect larvae) • Documentation of anaerobic cellulose decomposition by Omelianskii in 1902 • The study of sulfur-utilizing phototrophic bacteria by van Niel and others • The specificity of legume-nodulating bacteria (Fred et al., 1932) • The discovery and development of antibiotics • Direct microscopic methods of examining environmental microorganisms via staining and contactslide procedures • The development of radiotracer techniques • A diversity of advancements in analytical chemistry for detecting and quantifying biochemically and environmentally relevant compounds • Developments in molecular phylogeny (Woese, 1987, 1992; Pace, 1997) • The application of molecular methods to environmental microbiology (Olsen et al., 1986; Pace et al., 1986; Amann et al., 1991, 1995; Ward et al., 1993; White, 1994; van Elsas et al., 1997; Madigan and Martinko, 2006) 9781405136471_4_001.qxd 1/15/08 9:21 Page 9