Geomicrobiology 4th ed h ehrlich (dekker, 2001)

Preface to the Fourth EditionThe field of geomicrobiology has been receiving wider recognition than everbefore among environmental microbiologists and earth scientists since the firstappea

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GEOMICROBIOLOGY

Henry Lutz Ehrlich

Rensselaer Polytechnic Institute

Troy, New York

Fourth Edition, Revised and Expanded

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from whom I have learned as much

as I hope they have learned from me.

Preface to the Fourth Edition

The field of geomicrobiology has been receiving wider recognition than everbefore among environmental microbiologists and earth scientists since the firstappearance of the third edition of this book in November 1995 This is happeningbecause of an ever-increasing awareness of the influence of microbial activity inshaping the habitable part of our planet The pace of research on various aspects

of geomicrobiology in the last few years has significantly accelerated andproduced new discoveries of geomicrobial phenomena and yielded new insightsinto previously established phenomena The topic of geomicrobiology wasspecifically addressed in the program of recent annual meetings of the AmericanSociety of Microbiology (ASM) and, since the year 2000, has been allotted aspecial section in the table of contents of the journal Applied and EnvironmentalMicrobiology, published by ASM A journal exclusively devoted to the subject,the Geomicrobiology Journal, has been published independently of ASM since

1978 The timely publication of Geomicrobiology: Fourth Edition, Revised andExpanded, puts the new advances in the field in perspective

This fourth edition incorporates the important new findings of geomicrobialsignificance of the last five years Some of these findings were made by the

application of new physical and biological analytical techniques They enlargedour concept of the total size of the microbial habitat enormously because livingmicroorganisms have been detected below the Earth’s surface at significantlygreater depths than heretofore They have also expanded our understanding of thegreat diversity among the microbes in all the habitable parts of the Earth Intensiveinvestigations are ongoing to determine the interrelationships among the micro-organisms in these habitats and the nature of their activities from a geomicrobialstandpoint This edition reflects some modifications in the thinking about theorigin of life on Earth and its early evolution, but a divergence of views remains.

In regard to specific geomicrobial processes, the fourth edition reflects theincrease in our understanding of the microbial weathering of rocks and minerals

It contains a new chapter that deals with a probable role of microbes in theformation of bauxites The chapters on iron and manganese incorporate the latestfindings in regard to the physiology of microbial oxidation and reduction of ionicforms of these metals and some of their minerals and the diversity of theorganisms involved They also contain a more extensive discussion of themicrobial role in anaerobic biodegradation of organic carbon than in earliereditions The chapters dealing with sulfur, arsenic, and selenium compoundsincorporate the latest findings with regard to microbial oxidation and=or reduc-tion of corresponding forms of these elements The section on microbial metalsulfide oxidation in Chapter 19 has been extensively modified It reflects theimportant recent discovery that acidophilic Thiobacillus ferrooxidans (recentlyrenamed Acidithiobacillus ferrooxidans) seems to be a secondary rather than aprimary player in mobilizing metal from metal sulfide ores in heap-,dump-, and in situ leaching and in generating acid mine drainage, at least inmore advanced stages This chapter also examines a current controversy concern-ing the mechanism by which acidophilic iron bacteria oxidize metal sulfides Newreferences have been added to the chapter on the geomicrobiology of fossil fuels.The chief aim of the fourth edition of Geomicrobiology, like that of theearlier editions, is to serve as an introduction to the subject and to be of use as atext as well as an up-to-date reference book The book includes discussion of theolder literature as well as the recent literature, which is important for anappreciation of the development of the different areas of geomicrobiology As

in the earlier editions, the reference lists at the end of each chapter are notexhaustive but include the literature I deem most important Related literature can

be located by cross-referencing As in previous editions, a glossary is included toprovide definitions of scientific terms that may be unfamiliar to some readers

I have retained some of the drawings prepared by Stephen Chiang for thefirst edition A few illustrations from the third edition have been replaced, and afew entirely new ones have been added I am indebted to a number of persons andpublishers for making available original photographs or allowing reproduction of

previously published material They are acknowledged in the legends of theindividual illustrations.

I owe thanks to Donna Bedard for very helpful comments on the molecularaspects discussed in Chapter 7 My thanks also go to Jill Banfield, KatarinaEdwards, and Francisco F Roberto for reading Chapter 19, and to RonaldOremland for reading Chapters 13 and 20 I am indebted to Sigal Lechno-Yossef for help with the digital photomicrography setup in the biology depart-ment

The continued belief of Marcel Dekker, Inc., in the importance of this bookhas encouraged me greatly in preparing this fourth edition Special thanks go toSandra Beberman, Vice President, Medical Division; Michael Deters andMoraima Suarez, Production Editors; and the editorial staff

Responsibility for the presentation and interpretation of the subject matter

in this edition rests entirely with me

Henry Lutz Ehrlich

Preface to the Third Edition

The need for a third edition of Geomicrobiology has arisen because of someimportant advances in the field since the second edition Of particular significanceare advances in the areas of subsurface microbiology as it relates to groundwater,carbonate deposition, rock weathering, methylmercury formation, oxidation andreduction of iron and manganese, chromate reduction, oxidation and reduction ofmolybdenum, reduction of vanadate (V) and uranium (VI), oxidation andreduction of sulfur compounds, reduction of selenate and selenite, methanogen-esis, microbial attack of coal, and degradation of hydrocarbons These advanceshave been integrated into the treatment of these subjects The chapter dealing withthe biochemistry and physiology of geomicrobial processes has been updated toconvey the basis for our current understanding of how and why microbes areinvolved in these processes

Because this book is meant to serve as a reference as well as a textbook,very little material from the second edition has been eliminated By retaining thisinformation, an overview of the growth of the field of geomicrobiology since itsinception is retained It enables newcomers to learn what has been accomplished

in the field and to gain an introduction to the literature The literature citations on

the different subjects are not exhaustive, but include the most important ones,making it possible to locate other works by cross-referencing As in the previouseditions, a glossary is included to aid in the definition of unfamiliar scientificterms.

In preparing this edition, I have retained some of the line drawings prepared

by Stephen Chiang for the first edition that were also included in the secondedition Some other illustrations from the second edition have been replaced, and

a few entirely new illustrations have been included I am indebted to a number ofpersons and publishers for making available original photographs or allowingreproduction of previously published material They are acknowledged in thelegends of the individual illustrations

I wish to thank Marcel Dekker, Inc., for their continued belief in theimportance of this book by encouraging the preparation of this third edition Iwant to express special thanks to Bradley Benedict, Assistant Production Editor,and the editorial staff for their assistance in preparing this edition

Responsibility for the presentation and interpretation of the subject matter

in this edition rests entirely with me

Henry Lutz Ehrlich

Preface to the Second Edition

As in the first edition of this book, geomicrobiology is presented as a field distinctfrom microbial ecology and microbial biogeochemistry The stress remains onexamination of specific geomicrobial processes, microorganisms responsible forthem, and the pertinence of these processes to geology

Most chapters from the earlier edition have been extensively revised andupdated As far as possible, new discoveries related to geomicrobiology reported

by various investigators since the writing of the first edition have been integratedinto the new edition Two new chapters have been added, one on the geomicro-biology of nitrogen and the other on the geomicrobiology of chromium Thesecond chapter of the first edition has been divided into two to allow for a moreconcise development of the two topics: Earth as microbial habitat and the origin

of microbial life on Earth

In the new edition,Chapters 2– are intended to provide the backgroundneeded for understanding the succeeding chapters, which deal with specificaspects of geomicrobiology An understanding of microbial physiology andbiochemistry is very important for a full appreciation of how specific microbes

can act as geomicrobial agents For this reason,Chapter 6was extensively revisedfrom its antecedent,Chapter 5, in the first edition.

Like its predecessor, the present edition is meant to serve not only as a text,but also as a general introduction and guide to the geomicrobial literature formicrobiologists, ecologists, geologists, environmental engineers, mining engi-neers, and others interested in the subject The literature citations are not intended

to be exhaustive, but cross-referencing, especially in cited review articles, shouldlead the reader to many other pertinent references not mentioned in this book.Some of the revisions in this edition, especially those relating to bioener-getics, were significantly influenced by a number of stimulating informaldiscussions with my colleague and research collaborator John C Salerno

In preparing this edition, I have retained some of the line drawings byStephen Chiang I have, however, replaced many of the other illustrations, andadded some new ones that I prepared on a Macintosh Plus computer with CricketDraw and Cricket Graph applications I wish to thank the Voorhees ComputerCenter of Rensselaer Polytechnic Institute for allowing me to use the LaserPrinter Facility and George Clarkson for making the necessary arrangements.Once again, I am indebted to a number of persons and publishers for makingavailable original photographs or allowing reproduction of previously publishedmaterial They are acknowledged in the legends of the individual illustrations

I wish to thank Marcel Dekker, Inc., for deeming the subject matter of thisbook of sufficient continued importance to publish this second edition Specialthanks go to Judith DeCamp, Production Editor, and the editorial staff for theirhelp in bringing this edition to fruition

Responsibility for the presentation and interpretation of the subject matter

in this edition rests entirely with me

Henry Lutz Ehrlich

Preface to the First Edition

This book deals with geomicrobiology as distinct from microbial ecology andmicrobial biogeochemistry Although these fields overlap to some degree, eachemphasizes different topics (see Chapter 1) A reader of this book should not,therefore, expect to find extensive discussions of ecosystems, food chains,nutritional cycles, mass transfer, or man-made pollution problems as such,because these topics are not at the heart of geomicrobiology Geomicrobiology

is the study of the role that microbes play or have played in specific geologicalprocesses

This book arose out of a strong need I felt in teaching a course ingeomicrobiology As of this writing, no single text is available that deals withthe group of topics presented in this book Previously, students in my geomicro-biology course needed to be referred to the many primary publications on thevarious topics These publications are very numerous and are scattered among aplethora of journals and books that are often not readily available Some arewritten in languages other than English This book is an attempt to glean the basicgeomicrobial principles from this literature and to illustrate these principles withmany different examples

Some readers of this book will have a stronger background in Earth andmarine science than in microbial physiology, while others will have a strongerbackground in microbial physiology than in Earth and marine sciences To enableall these readers to place the geomicrobial discussions in the later chapters inproper context, the introductoryChapters 2– were written They are not meant to

be definitive treatises on their subjects, and as a result any one of them will appearelementary to a person already knowledgeable in its field However, I have foundthe material in these chapters to be essential in teaching my students

As for the rest of the book, Chapter 6 summarizes the methods used ingeomicrobiology, andChapters 7–17examine specific geomicrobial activities inrelation to geologically important classes of substance or elements A single basictheme pervades these last 11 chapters: biooxidation and bioreduction and=orbioprecipitation and biosolution This may seem an unnecessary reiteration of acommon set of principles, but closer examination will show that the manifesta-tions of these principles in different geomicrobial phenomena differ so strikingly

as to require separate examination In discussing geomicrobial processes, I havetended to emphasize the physiological more than the geological aspects This is inpart because the former is my own area of greater expertise, but also, and moreimportantly, because I feel that the physiological and biochemical nature ofgeomicrobial processes has to be understood to fully appreciate why somemicrobes are capable of these activities

In citing microorganisms in the text, the names employed by the gators whose work is described are used In the case of bacteria, these names mayhave subsequently changed The currently used names of the bacteria may befound by referring to Bergey’s Manual of Determinative Bacteriology (8thedition, edited by R E Buchanan and N E Gibbons, 1974, Williams andWilkins, Baltimore) and to the Index Bergeyana (R E Buchanan, J G Holt, and

investi-E F Lessel, 1966, Williams and Wilkins, Baltimore) In some instances,however, it may be impossible to find a bacterial organism listed in the Manual

or the Index because the organism was never sufficiently described to achievetaxonomic status The current names of renamed bacteria may also be found inthe index of organisms at the end of this book

It is hoped that this book will serve not only as a text but also as anintroduction and guide to the geomicrobiological literature for microbiologists,ecologists, geologists, environmental engineers, and others interested in thesubject

The preparation of this book was greatly aided by discussion with, andreview of the manuscript by, Galen E Jones, R Schweisfurth, William C.Ghiorse, Edward J Arcuri, Paul A LaRock, and many students in my geo-microbiology course Responsibility for the presentation and interpretation of thesubject matter as found in this book rests, however, entirely with me I amindebted to a number of persons and publishers for making available original

photographs or allowing reproduction of previously published material forillustration They are acknowledged in the legends of the individual illustrations.

I wish to thank Stephen Chiang for his preparation of finished line drawings fromthe crude sketches I furnished I also wish to thank the editorial staff of MarcelDekker, Inc., for their help in readying my manuscript for publication

Henry Lutz Ehrlich

Contents

3 The Origin of Life and Its Early History 21

6.2 Geomicrobially Important Physiological Groups of

6.3 Role of Microbes in Inorganic Conversions in the

6.4 Types of Microbial Activities Influencing Geological

6.5 Microbes as Catalysts of Geochemical Processes 123

6.7 Microbial Products of Metabolism That Can Cause

6.8 Physical Parameters That Influence Geomicrobial Activity 144

7 Methods in Geomicrobiology 153

7.2 Detection and Isolation of Geomicrobially Active Organisms 1557.3 In Situ Study of Past Geomicrobial Activity 1647.4 In Situ Study of Ongoing Geomicrobial Activity 1667.5 Laboratory Reconstruction of Geomicrobial Processes in

7.7 Test for Distinguishing Between Enzymatic and

7.8 Study of Reaction Products of a Geomicrobial

8.4 Biological Carbonate Formation and Degradation and

9.2 Biologically Important Properties of Silicon and Its

11 Geomicrobial Interactions with Phosphorus 267

11.3 Conversion of Organic into Inorganic Phosphorus and the

11.5 Microbial Solubilization of Phosphate Minerals 271

11.7 Microbial Reduction of Oxidized Forms of Phosphorus 27811.8 Microbial Oxidation of Reduced Forms of Phosphorus 280

12 Geomicrobially Important Interactions with Nitrogen 289

14.5 Specific Microbial Interactions with Mercury 33014.6 Genetic Control of Mercury Transformations 33514.7 Environmental Significance of Microbial Mercury

15 Geomicrobiology of Iron 345

15.6 Iron(III) as Terminal Electron Acceptor in Bacterial

15.7 Nonenzymatic Oxidation of Ferrous Iron and Reduction

15.10 Sedimentary Iron Deposits of Putative Biogenic Origin 39815.11 Microbial Mobilization of Iron from Minerals in Ore,

16.4 Manganese-Oxidizing and -Reducing Bacteria and Fungi 431

17 Geomicrobial Interactions with Chromium, Molybdenum,

18.2 Geochemically Important Properties of Sulfur 550

18.4 Mineralization of Organic Sulfur Compounds 551

18.6 Geomicrobially Important Types of Bacteria That React

18.7 Physiology and Biochemistry of Microbial Oxidation of

18.8 Autotrophic and Mixotrophic Growth on Reduced Forms

19.4 Laboratory Evidence in Support of Biogenesis of Metal

19.6 Bioleaching of Metal Sulfide and Uraninite Ores 642

19.7 Bioextraction of Metal Sulfide Ores by Complexation 651

20.4 Bio-oxidation of Reduced Forms of Selenium 67120.5 Bioreduction of Oxidized Selenium Compounds 672

Introduction

Geomicrobiology examines the role that microbes have played in the past and arecurrently playing in a number of fundamental geological processes Examples ofsuch processes are the weathering of rocks, soil and sediment formation andtransformation, the genesis and degradation of minerals, and the genesis anddegradation of fossil fuels Geomicrobiology should not be equated with micro-bial ecology or microbial biogeochemistry Microbial ecology is the study ofinterrelationships between different microorganisms; among microorganisms,plants, and animals; and between microorganisms and their environment Micro-bial biogeochemistry is the study of microbially influenced geochemical reac-tions, enzymatically catalyzed or not, and their kinetics These reactions are oftenstudied in the context of mineral cycles, with emphasis on environmental masstransfer and energy flow These three subjects do overlap to some degree, asshown in Figure 1.1

The origin of the word ‘‘geomicrobiology’’ is obscure It obviously derivedfrom the term ‘‘geological microbiology.’’ Beerstecher (1954) defined geomicro-biology as ‘‘the study of the relationship between the history of the Earth andmicrobial life upon it.’’ Kuznetsov et al (1963) defined it as ‘‘the study ofmicrobial processes currently taking place in the modern sediments of variousbodies of water, in ground waters circulating through sedimentary and igneousrocks, and in weathered Earth crust [and also] the physiology of specific

microorganisms taking part in presently occurring geochemical processes.’’Neither author traced the history of the word, but they pointed to the importantroles that scientists such as Winogradsky, Waksman, and ZoBell played in thedevelopment of the field.

Geomicrobiology is not a new field, although until the last few years it didnot receive much attention Certain early investigators in soil and aquaticmicrobiology may not have thought of themselves as geomicrobiologists, butthey nevertheless had an influence on the subject One of the first contributors togeomicrobiology was Ehrenberg (1838), who in the second quarter of thenineteenth century discovered the association of Gallionella ferruginea withochreous deposits of bog iron He believed that the organism, which he thought to

be an infusorian but which we now recognize as a stalked bacterium, wasimportant in the formation of such deposits Another important early contributor

to geomicrobiology was Winogradsky, who discovered that Beggiatoa couldoxidize H2S to elemental sulfur (1887) and that Leptothrix ochracea promotedoxidation of FeCO3 to ferric oxide (1888) He believed that both organismsgained energy from these processes Still other important early contributors togeomicrobiology were Harder (1919), a researcher trained as a geologist andmicrobiologist, who studied the significance of microbial iron oxidation andprecipitation in relation to the formation of sedimentary iron deposits, and Stutzer(1912), Vernadsky (1908–1922)(1955), and others, whose studies led to recogni-tion of the significance of microbial oxidation of H2S to elemental sulfur in theformation of sedimentary sulfur deposits [see Ivanov (1967), Lapo (1987), and

FIG. 1.1 Interrelationships among geomicrobiology, microbial ecology, microbialbiogeochemistry, and biogeochemistry

Bailes (1990) for a discussion of early Russian geomicrobiology and its tioners] Our understanding of the role of bacteria in sulfur deposition in naturereceived a further boost from the discovery of bacterial sulfate reduction byBeijerinck (1895) and van Delden (1903).

practi-Starting with the Russian investigator Nadson (1903) (see also Nadson,1928) at the end of the nineteenth century, and continuing with such investigators

as Bavendamm (1932), the important role of microbes in CaCO3 precipitationbegan to be noted Microbial participation in manganese oxidation and precipita-tion in nature was first indicated by Beijerinck (1913), Soehngen (1914), Lieske(1919), and Thiel (1925) Zappfe (1931) later related this activity to the formation

of sedimentary manganese ore The microbial role in methane formation becameapparent through the observations and studies of Be´champ (1868), Tappeiner(1882), Popoff (1875), Hoppe-Seyler (1886), Omeliansky (1906), and Soehngen(1906); see also Barker (1956) The role of bacteria in rock weathering was firstsuggested by Muentz (1890) and Merrill (1895) Later, involvement of acid-producing microorganisms such as nitrifiers and of crustose lichens and fungi wassuggested (see Waksman, 1932) Thus by the beginning of the twentieth century,many of the important areas of geomicrobiology had begun to receive seriousattention from microbiologists In general, it may be said that most of thegeomicrobiologically important discoveries of the nineteenth century weremade through physiological studies in the laboratory that revealed the capacity

of specific organisms for geomicrobiologically important transformations, ing later workers to study the extent of the microbial activities in the field.Geomicrobiology in the United States can be said to have begun with thework of E C Harder (1919) on iron-depositing bacteria Other early Americaninvestigators of geomicrobial phenomena include J Lipman, S A Waksman,

caus-R L Starkey, and H O Halvorson, all prominent in soil microbiology, and

G A Thiel, C Zappfe, and C E ZoBell, all prominent in aquatic microbiology.ZoBell was a pioneer in marine microbiology (Ehrlich, 2000)

Very fundamental discoveries in geomicrobiology continue to be made,some basic ones having been made as the twentieth century progressed and othersvery recently For instance, the concept of environmental limits of pH and Eh formicrobes in their natural habitats was first introduced by Baas Becking et al.(1960) (see Chap 6) Life at high temperature in nature was systematicallystudied for the first time in the 1970s by Brock and associates in YellowstonePark, in the United States (Brock, 1978) A specific acidophilic, iron-oxidizingbacterium and its association with the production of acid coal mine drainage wasfirst discovered in the late 1940s, the result of studies by Colmer et al (1950) (seeChaps 15and19) The subsequent demonstration of the presence of these sameorganisms in acid mine drainage from a copper sulfide ore body in Utah(Bingham Canyon open pit mine) and the experimental finding that theseorganisms can promote the leaching of metals from various metal sulfide ores

(Bryner et al., 1954) led to the first industrial application of geomicrobially activeorganisms (Zimmerley et al., 1958) (Chap 19) The first attempts at visualdetection of Precambrian prokaryotic fossils in sedimentary rocks were made byTyler and Barghoorn in 1954 and by Schopf et al and by Barghoorn and Schopf

in 1965 (see Chap 3) Paleontological discoveries resulting from these studieshave had a profound influence on current theories about the evolution of life onEarth (Schopf, 1983) The discovery of geomicrobially active microorganismsaround submarine hydrothermal vents (Jannasch and Mottl, 1985; Tunnicliffe,1992) and the demonstration of a significant viable microflora with the potentialfor geomicrobially important activity in the deep subsurface of continents(Ghiorse and Wilson, 1988; Sinclair and Ghiorse, 1989; Fredrickson et al.,1989; Pederson, 1993) and the ocean floor (Parkes et al., 1994) are opening uppreviously unsuspected new topics for geomicrobial study

As this book will show, many areas of geomicrobiology remain to be fullyexplored or developed further

Be´champ E 1868 Ann Chim Phys 13:103 (as cited by Barker, 1956)

Beerstecher E 1954 Petroleum Microbiology New York: Elsevier

Beijerinck MW 1895 U¨ ber Spirillum desulfuricans als Ursache der Sulfatreduktion.Zentralbl Bakteriol Parasitenk Infektionskr Hyg Abt I Orig 1:1–9, 49–59, 104–114.Beijerinck MW 1913 Oxydation des Mangancarbonates durch Bakterien und Schimmel-pilzen Folia Microbiol (Delft) 2:123–134

Brock TD 1978 Thermophilic Microorganisms and Life at High Temperatures New York:Springer-Verlag

Bryner LC, Beck JV, Davis DB, Wilson DG 1954 Microorganisms in leaching sulfideminerals Ind Eng Chem 46:2587–2592

Colmer AR, Temple KL, Hinkle HE 1950 An iron-oxidizing bacterium from the aciddrainage of some bituminous coal mines J Bacteriol 59:317–328

Ehrenberg CG 1838 Die Infusionsthierchen als vollkommene Organismen Leipzig,Germany: L Voss

Ehrlich HL 2000 ZoBell and his contributions to the geosciences 2000 In: Bell CR,Brylinsky M, Johnson-Green P, eds Microbial Biosystems: New Frontiers Proc 8th Int

Symp Microb Ecol Atlantic Canada Society for Microbial Ecology, Halifax, Canada,vol 1, pp 57–62.

Fredrickson JK, Garland TR, Hicks RJ, Thomas JM, Li SW, McFadden K 1989.Lithotrophic and heterotrophic bacteria in deep subsurface sediments and their relation

to sediment properties Geomicrobiol J 7:53–66

Ghiorse WC, Wilson JT 1988 Microbial ecology of the terrestrial subsurface Adv ApplMicrobiol 33:107–172

Harder EC 1919 Iron depositing bacteria and their geologic relations US Geol Surv ProfPap 113

Hoppe-Seyler FZ Physiol Chem 1886 10:201, 401 (as cited by Barker, 1956)

Ivanov MV 1967 The development of geological microbiology in the U.S.S.R biologiya 31:795–799

Mikro-Jannasch HW, Mottl MJ 1985 Geomicrobiology of the deep sea hydrothermal vents.Science 229:717–725

Kuznetsov SI, Ivanov MV, Lyalikova NN 1963 Introduction to Geological Microbiology.English transl New York: McGraw-Hill

Lapo AV 1987 Traces of Bygone Biospheres Moscow: Mir Publishers

Lieske R 1919 Zur Erna¨hrungsphysiologie der Eisenbakterien Zentralbl BakteriolParasitenk Infektionskr Hyg Abt II 49:413–425

Merrill GP 1895 Geol Soc Am Bull 6:321–332 (as cited by Waksman, 1932)

Muentz A 1890 Sur la de´composition des roches et la formation de la terre arable CRAcad Sci (he´bd se´ances) (Paris) 110:1370–1372

Nadson GA 1903 Microorganisms as Geologic Agents I Tr Komisii Isslect Min Vodg StPetersburg: Slavyanska, 1903

Nadson GA 1928 Beitrag zur Kenntnis der bakteriogenen Kalkablagerung Arch biol 19:154–164

Hydro-Omeliansky W 1906 Zentralbl Bakteriol Parasitenk Infektionskr Hyg Abt II 15:673 (ascited by Barker, 1956)

Parkes RJ, Cragg BA, Bale SJ, Getliff JM, Goodman K, Rochelle PA, Fry JC, Weightman

AJ, Harvey SM 1994 Deep bacterial biosphere in Pacific Ocean sediments Nature(Lond) 371:410–413

Pedersen K 1993 The deep subterranean biosphere Earth-Sci Rev 34:243–260.Popoff L 1875 Arch Ges Physiol 10:142 (as cited by Barker, 1956)

Schopf JW, ed 1983 Earth’s Earliest Biosphere Its Origin and Evolution Princeton, NJ:Princeton Univ Press

Schopf JW, Barghoorn ES, Maser MD, Gordon RO 1965 Electron microscopy of fossilbacteria two billion years old Science 149:1365–1367

Sinclair JL, Ghiorse WC 1989 Distribution of aerobic bacteria, protozoa, algae, and fungi

in deep subsurface sediments Geomicrobiol J 7:15–31

Soehngen NL 1906 Het oustaan en verdwijnen van waterstof en methaan ouder invloedvan het organische leven Thesis Technical Univ, Delft Delft, Netherlands: Vis, Jr.Soehngen NL 1914 Umwandlung von Manganverbindungen unter dem Einfluss mikro-biologischer Prozesse Zentralbl Bakteriol Parasitenk Infektionskr Hyg Abt II 40:545–554

Stutzer O 1912 Origin of sulfur deposits Econ Geol 7:733–743

Tappeiner W 1882 Ber Deut Chem Ges 15:999 (as cited by Barker, 1956).

Thiel GA 1925 Manganese precipitated by microorganisms Econ Geol 20:301–310.Tunnicliffe V 1992 Hydrothermal-vent communities of the deep sea Am Sci 80:336–349.Tyler SA, Barghoorn ES 1954 Occurrence of structurally preserved plants in Precambrianrocks of the Canadian Shield Science 119:606–608

van Delden A 1903 Beitrag zur Kentnis der Sulfatreduktion durch Bakterien ZentralblBakteriol Parasitenk Infektionskr Hyg Abt II 11:81–94

Vernadsky VI 1955 An Attempt at Descriptive Mineralogy Izbrannye Trudy, Vol 2.Izdatel’stvo Moscow: Akad Nauk SSSR

Waksman SA 1932 Principles of Soil Microbiology 2nd ed rev Baltimore, MD: William

& Wilkins

Winogradsky S 1887 U¨ ber Schwefelbakterien Bot Ztg 45:489–600

Winogradsky S 1888 U¨ ber Eisenbakterien Bot Ztg 46:261–276

Zappfe C 1931 Deposition of manganese Econ Geol 26:799–832

Zimmerley SR, Wilson DG, Prater JD 1958 Cyclic leaching process employing ironoxidizing bacteria US Patent 2,829,964

The Earth as a Microbial Habitat

2.1 GEOLOGICALLY IMPORTANT FEATURES

The interior of the planet Earth consists of three successive regions (Fig 2.1), theinnermost being the core It is surrounded by the mantle, which, in turn, issurrounded by the outermost region, the crust The crust is surrounded by agaseous envelope, the atmosphere

The core, whose radius is estimated to be about 3450 km, is believed toconsist of an Fe-Ni alloy with an admixture of small amounts of the siderophileelements cobalt, rhenium, and osmium, very probably some sulfur and phos-phorus, and perhaps even hydrogen (Mercy, 1972; Anderson, 1992; Wood, 1997).The inner portion of the core, which has an estimated radius of about 1250 km, issolid, having a density of 13 g cm
3 and being subjected to a pressure of

3:7  1012dyn cm
2 The outer portion of the core has a thickness of about

2200 km and is molten, owing to the higher temperature but lower pressure than

at the central core (1.3–3.21012dyn cm
2) The density of this portion is 9.7–12.5 g cm
3

The mantle, which has a thickness of about 2865 km, has a very differentcomposition from the core and is separated from it by the Wickert–Gutenbergdiscontinuity (Madon, 1992) Seismic measurements of the mantle regions haverevealed distinctive regions called the upper mantle (365 km thick), transitionzone (270 km thick), and lower mantle (1230 km thick) (Madon, 1992) The

mantle rock is dominated by the elements O, Mg, and Si with lesser amounts of

Fe, Al, Ca, and Na (Mercy, 1972) The consistency of the rock in the uppermantle, although not truly molten, is thought to be plastic, especially in the regioncalled the asthenosphere, situated 100–220 km below the Earth’s surface(Madon, 1992) Upper mantle rock penetrates the crust on rare occasions andmay be recognized as an outcropping, as in the case of some ultramafic rock onthe bottom of the western Indian Ocean (Bonatti and Hamlyn, 1978)

The crust is separated from the mantle by the Mohorovicˇic discontinuity.The thickness of the crust varies from as little as 5 km under ocean basins to asgreat as 70 km under continental mountain ranges The average crustal thickness

is 45 km (Madon, 1992; Skinner et al., 1999) The rock of the crust is dominated

by O, Si, Al, Fe, Mg, Na, and K (Mercy, 1972) These elements make up 98.03%

FIG.2.1 Diagrammatic cross section of the Earth Radii of core and mantle drawn toscale

of the weight of the crust (Skinner et al., 1999) and occur predominantly in therocks and sediments The bedrock under the oceans is generally basaltic, whereasthat of the continents is granitic to an average crustal depth of 25 km Below thisdepth it is basaltic to the Mohorovicˇic discontinuity (Ronov and Yaroshevsky,

1972, p 243) Sediment covers most of the bedrock under the oceans It ranges inthickness from 0 to 4 km Sedimentary rock and sediment (soil in a nonaquaticcontext) cover the bedrock of the continents; their thickness may exceed that ofmarine sediments (Kay, 1955, p 655) The continents make up 64% of the crustalvolume, the oceanic crust makes up 21%, and the shelf and subcontinental crustmake up the remaining 15% (Ronov and Yaroshevsky, 1972)

Although until the 1960s it was usually viewed as a coherent structure thatrests on the mantle, the Earth’s crust is now seen to consist of a series of movingand interacting plates of varying sizes and shapes Some plates support thecontinents and parts of the ocean floor, whereas others support only parts of theocean floor The present estimate of the number of major plates involved is stillnot fully agreed upon but ranges from 10 to 12 (Keary, 1993) to 16 according tothe National Geographic Society (1995) Figure 2.2 shows the outlines of some ofthe major plates and adjacent continents The plates float on the asthenosphere ofthe mantle The crust plus the upper mantle above the asthenosphere is sometimesreferred to as the lithosphere by geologists Convection resulting from the thermalgradients in the plastic rock of the asthenosphere is believed to be the cause ofmovement of the crustal plates (e.g., Kerr, 1995; Wysession, 1995; Ritter, 1999)

In some locations this movement may manifest itself in collision of plates, in

FIG.2.2 Major crustal plates of the Earth

other locations in a sliding past each other along transform faults, and in stillother locations in sliding over each other The last process is called subduction(crustal convergence) It may result when a denser oceanic plate slides below alighter continental plate, or when adjacent oceanic plates of nearly equal densityinteract Either interaction may lead to formation of a trench–volcanic island arcsystem In the case of oceanic–continental plate collisions, the resulting arcsystem may eventually accrete to the continental margin as a result of themovement of the subducting oceanic plate in the direction of the continentalplate The island arc system results from a sedimentary wedge formed by theoceanic plate (Van Andel, 1992; Gurnis, 1992).

Oceanic plates grow along oceanic ridges, the sites of crustal divergence.Examples are the Mid-Atlantic Ridge and the East Pacific Rise (Fig 2.3) Theoldest portions of growing oceanic plates are destroyed through subduction withthe formation of deep-sea trenches, such as the Marianas, Kurile, and Philippinetrenches in the Pacific Ocean and the Puerto Rico Trench in the Atlantic Ocean.Growth of the oceanic plates at the mid-ocean ridges is the result of submarinevolcanic eruptions of magma (molten rock from the deep crust or upper mantle).This magma is added to opposing plate margins along a mid-ocean ridge, causing

FIG.2.3 Major mid-ocean rift system (thin continuous lines) and ocean trenches (heavycontinuous lines) A, Philippine Trench; B, Marianas Trench; C, Vityaz Trench; D, NewHebrides Trench; E, Peru–Chile Trench; F, Puerto Rico Trench The East Pacific Ridge isalso known as the East Pacific Rise

adjacent parts of the plates to be pushed away from the ridge in oppositedirections (Fig 2.4) The oldest portions of oceanic plates are consumed bysubduction more or less in proportion to the formation of new oceanic plate at themid-ocean ridges, thereby maintaining a fairly constant plate size.

Volcanism occurs not only at mid-ocean ridges but also in the regions ofsubduction where the sinking crustal rock undergoes melting as it descendstoward the upper mantle The molten rock may then erupt through fissures in thecrust and contribute to mountain building at the continental margins (orogeny) It

is plate collision and volcanic activity associated with subduction at continentalmargins that accounts mainly for the existence of coastal mountain ranges Theorigin of the Rocky Mountains and the Andes on the North and South Americancontinents, respectively, is associated with subduction activity, whereas theHimalayas are the result of collision of the plate holding the Indian subcontinentwith that holding the Asian continent

Volcanic activity may also occur away from crustal plate margins, atso-called hot spots In the Pacific Ocean, one such hot spot is represented bythe island of Hawaii with its active volcanoes The remainder of the Hawaiianisland chain had its origin at the same hot spot where the island of Hawaii ispresently located Crustal movement of the Pacific Ocean plate westward caused

FIG. 2.4 Schematic representation of seafloor spreading and plate subduction Newoceanic crust is formed at the rift zone of the mid-ocean ridge Old oceanic crust isconsumed in the subduction zone near a continental margin or island arc

the remaining islands to be moved away from the hot spot so that they are nolonger volcanically active.

The continents as they exist today are thought to have derived from a singlecontinental mass, Pangaea, which broke apart due to crustal movement less than

200 million years ago Initially this separation gave rise to Laurasia (whichincluded present-day North America, Europe, and most of Asia) and Gondwana(which included present-day Africa, South America, Australia, Antarctica, andthe Indian subcontinent) These continents separated subsequently into thecontinents we know today, except for the Indian subcontinent, which did notjoin the Asian continent until some time after this breakup (Fig 2.5) (Dietz andHolden, 1970; Fooden, 1972; Matthews, 1973; Palmer, 1974; Hoffman, 1991;Smith, 1992) The continents that evolved became modified by accretion of smalllandmasses through collision with plates bearing them Pangaea itself is thought

to have originated 250–260 million years ago from an aggregation of crustalplates bearing continental landmasses including Baltica (consisting of Russiawest of the Ural Mountains, Scandinavia, Poland, and Northern Germany), China,Gondwana, Kazakhstania (consisting of present-day Kazakhstan), Laurentia(consisting of most of North America, Greenland, Scotland, and the ChukotskiPeninsula of eastern Russia), and Siberia (Bambach et al., 1980) Mobilecontinental plates are believed to have existed as long as 3.5 billion years ago(Kroener and Layer, 1992)

The evidence for the origin and movement of the present-day continentsrests on at least three kinds of studies: paleomagnetic and seismic examinations ofthe Earth’s crust, comparative sedimentary analyses of deep-ocean cores obtainedfrom drillings by the Glomar Challenger, an ocean-going research vessel, andpaleoclimatic studies (Bambach et al., 1980; Nierenberg, 1978; Vine, 1970;Ritter, 1999) Although the separation of the present-day continents had probably

no significant effect on the evolution of prokaryotes (they had pretty muchevolved to their present complexity by this time), it did have a profound effect onthe evolution of metaphytes and metazoans (McKenna, 1972; Raven and Axelrod,1972) Flowering plants, birds, and mammals, for example, had yet to establishthemselves

The biosphere, that portion of the planet that supports life, is restricted to theuppermost part of the crust and, to a degree, to the lowermost part of theatmosphere It includes the land surface, i.e., the exposed sediment or soil androck to a limited depth, sometimes called the lithosphere by ecologists (seeSec 2.1for geologists’ definition), and the hydrosphere, that portion of the crustcovered by water Although on land most life exists at the surface, significant

populations of microbes have now been detected in various sedimentary rockstrata at depths of hundreds of meters and more (Ghiorse and Wilson, 1988;Pedersen, 1993) Life in the exposed crust or lithosphere on land was claimed byPokrovskiy (cited by Kuznetsov et al., 1963, p 26) to exist to a depth as great as

FIG. 2.5 Continental drift Simplified representation of the breakup of Pangaea topresent time (Reproduced from Dietz and Holden, 1970.)

4000 m Much more recently, a controlled study confirmed the presence of life ingroundwater from a depth of 3500 m from a borehole in granitic rock in the SiljanRing in central Sweden (Szewzyk et al., 1994) The water from this depthcontained thermophilic, anaerobic fermenting bacteria related to Thermo-anaerobacter and Thermoanaerobium species and one strain related to Clostri-dium thermohydrosulfuricum but no sulfate-reducing or methanogenic bacteria.The bacteria that were cultured grew in a temperature range of 45–75C (65Coptimum) at atmospheric pressure in the laboratory In continental crust, thetemperature has been estimated to increase by about 25C per kilometer of depth(Fredrickson and Onstott, 1996) Using this constant, the in situ temperature at adepth of 3500 m should be about 87:5C, which is higher than the maximumtemperature tolerated by the cultures isolated by Szewzyk et al (1994) whengrown under laboratory conditions, but well within the temperature range ofhyperthermophilic bacteria (present maximum growth temperature about 110C).Within a very limited range, elevated hydrostatic pressure to which microbeswould be subjected at greater depths may increase their temperature toleranceslightly, as suggested by the observations of Haight and Morita (1962) and Moritaand Haight (1962) Clearly temperature and hydrostatic pressure are importantdeterminants of the depth limit at which life can exist within the crust Otherimportant limiting factors are porosity and the availability of nutrients andmoisture (Colwell et al., 1997).

Unlike the lithosphere, the hydrosphere is inhabited by life at all waterdepths, some as great as 11,000 m, the depth of the Marianas Trench In marinesediments, microbial life has now been detected at depths of>500 mbsf (metersbelow the surface) (Parkes et al., 1994; Cragg et al., 1996) Bacterial alteration ofthe glass in ocean basalts has been seen to decreasing extents for 250–500 mbsf(Torsvik et al., 1998; Furnes and Staudigel, 1999) In some parts of the hydro-sphere, some special ecosystems have evolved whose primary energy source isgeothermal rather than radiant energy from the sun (Jannasch, 1983) Theseecosystems occur around hydrothermal vents at mid-ocean rift zones Here heatfrom magma chambers diffuses upward into overlying basalt, causing seawaterthat has penetrated deep into the basalt to react with it (see Chap 16,Fig 16.17,for a diagrammatic representation of this process) This seawater–basalt interac-tion results in the formation of hydrogen sulfide and in the solution of somemetals, particularly iron and manganese and in some cases some other metalssuch as copper and zinc The altered seawater (now a hydrothermal solution)charged with these solutes is eventually forced up through cracks and fissures inthe basalt to enter the overlying ocean through hydrothermal vents Autotrophicbacteria living free around the vents or in symbiotic association with somemetazoa at these sites use the hydrogen sulfide as an energy source for convertingcarbon dioxide into organic matter Some of this organic matter is used as food byheterotrophic microorganisms and metazoa at these locations (Jannasch, 1983;

Tunnicliffe, 1992) The hydrogen sulfide–oxidizing bacteria are the chiefprimary producers in the ecosystems, taking the place of photosynthesizerssuch as cyanobacteria, algae, or plants, the usual primary producers on Earth.Photosynthesizers cannot operate in the location of hydrothermal vent commu-nities because of the perpetual darkness that prevails at these sites (see also Chap.

18,Sec 18.8)

Not all submarine communities featuring chemosynthetic hydrogen sulfideoxidizers as primary producers are based on hydrothermal discharge On theFlorida Escarpment in the Gulf of Mexico, ventlike biological communities havebeen found at abyssal depths around hydrogen sulfide seeps whose discharge is atambient temperature The sulfide in this instance may originate from an adjacentcarbonate platform containing fluids with 250% dissolved solids and tempera-tures up to 115C (Paul et al., 1984)

In some other instances, such as the Oregon Subduction Zone or at somesites on the Florida Escarpment, methane of undetermined origin expelled fromthe pore fluids of the sediments, rather than hydrogen sulfide, is the basis forprimary production on the seafloor Metazoa share in the carbon fixed by free-living or symbiotic methane-oxidizing bacteria (Kulm et al., 1986; Childress

et al., 1986; Cavanaugh et al., 1987) (see alsoChap 21)

Finally, the biosphere includes the lower portion of the atmosphere Livingmicrobes have been recovered from it at heights as great as 48–77 km above theEarth’s surface (Imshenetsky et al., 1978; Lysenko, 1979)

Whether the atmosphere constitutes a true microbial habitat is verydebatable Although it harbors viable vegetative cells and spores, it is generallynot capable of sustaining growth and multiplication of these organisms because oflack of sufficient moisture and nutrients and because of lethal radiation, especially

at higher elevations At high humidity in the physiological temperature range,some bacteria may, however, propagate to a limited extent (Dimmick et al., 1979;Straat et al., 1977) The residence time of microbes in air may also be limited,owing to eventual fallout In the case of microbes associated with solid particlessuspended in still air, the fallout rate may range from 10
3cm sec
1for particles

in a 0.5mm size range to 2 cm sec
1 for particles in a 10mm size range (Brock,

1974, p 541) Even if it is not a true habitat, the atmosphere is neverthelessimportant to microbes It is a vehicle for spreading microbes from one site toanother; it is a source of oxygen for strict and facultative aerobes; it is a source ofnitrogen for nitrogen-fixing microbes; and its ozone layer screens out most of theharmful ultraviolet radiation from the sun

Although the biosphere is restricted to the uppermost crust and the sphere, the core of the Earth does exert an influence on some forms of life Thecore, with its solid center and molten outer portion, acts like a dynamo ingenerating the magnetic field surrounding the Earth (Strahler, 1976, p 36;Gubbins and Bloxham, 1987; Su et al., 1996; Glatzmaier and Roberts, 1996)

atmo-Magnetotactic bacteria, because they form magnetite or iron sulfide crystals intheir cells that behave like compasses, can utilize the Earth’s magnetic field forpurposes of orientation in seeking their preferred habitat, which is a partiallyreduced environment They are able to align themselves with respect to theEarth’s magnetic field (Blakemore, 1982; DeLong et al., 1993).

The surface of the Earth includes the lithosphere, hydrosphere, and atmosphere,all of which are habitable by microbes to a greater or lesser extent and constitutethe biosphere of the Earth

The structure of the Earth can be separated into the core, the mantle, andthe crust Of these, only the uppermost portion of the crust is habitable by livingorganisms The crust is not a continuous solid layer over the mantle, but consists

of a number of crustal plates afloat on the mantle, or more specifically on theasthenosphere of the mantle Some of the plates lie entirely under the oceans.Others carry parts of a continent or parts of a continent and an ocean Oceanicplates are growing along mid-ocean spreading centers, while old portions arebeing destroyed by subduction under or collision with continental plates Thecrustal plates are in constant, albeit slow, motion owing to the action ofconvection cells in the underlying mantle The plate motion accounts forcontinental drift

REFERENCES

Anderson DL 1992 The earth’s interior In: Brown CG, Hawksworth CJ, Wilson RCL,eds Understanding the Earth Cambridge, UK: Cambridge Univ Press, pp 44–66.Bambach RK, Scotese CR, Ziegler AF 1980 Before Pangaea: The geography of thePaleozoic world Am Sci 68:26–38

Blakemore RP 1982 Magnetotactic bacteria Annu Rev Microbiol 36:217–238.Bonnatti E, Hamlyn PR 1978 Mantle uplifted block in western Indian Ocean Science201:249–251

Brock TD 1974 Biology of Microorganisms 2nd ed Englewood Cliffs, NJ: Prentice-Hall.Cavanaugh CM, Levering PR, Maki JS, Mitchell R, Lidstrom ME 1987 Symbiosis ofmethylotrophic bacteria and deep-sea mussels Nature (Lond) 325:346–348

Childress JJ, Fischer CR, Brooks JM, Kennecutt MC II, Bidigare R, Anderson AE 1986

A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: Mussels fueled

by gas Science 233:1306–1308

Colwell FS, Onstott TC, Delwiche ME, Chandler D, Fredrickson JK, Yao Q-J, McKinley

JP, Boone DR, Griffiths R, Phelps TJ, Ringelberg D, White DC, LaFreniere L, Balkwill

D, Lehman RM, Konisky J, Long PE 1997 Microorganisms from deep, hightemperature sandstones: Constraints on microbial colonization FEMS Microbiol Rev20:425–435

Cragg BA, Parkes RJ, Fry JC, Weightman AJ, Rochelle PA, Maxwell JR 1996 Bacterialpopulations and processes in sediments containing gas hydrates (OPD Leg 146:Cascadia Margin) Earth Planet Sci Lett 139:497–507.

DeLong EF, Frankel RB, Bazylinski DA 1993 Multiple evolutionary origin of totaxis Science 259:803–806

magne-Dietz RC, Holden JC 1970 Reconstruction of Pangaea: Breakup and dispersion ofcontinents, Permian to present J Geophys Res 75:4939–4956

Dimmick RL, Wolochow H, Chatigny MA 1979 Evidence that bacteria can form newcells in air-borne particles Appl Environ Microbiol 37:924–927

Fooden J 1972 Breakup of Pangaea and isolation of relict mammals in Australia, SouthAmerica, and Madagascar Science 175:894–898

Fredrickson JK, Onstott TC 1996 Microbes deep inside the Earth Sci Am 275:68–83

Furnes H, Staudigel H 1999 Biological mediation in ocean crust alteration: How deep isthe deep biosphere? Earth Planet Sci Lett 166:97–103

Ghiorse WC, Wilson JT 1988 Microbial ecology of the terrestrial subsurface Adv ApplMicrobiol 33:107–171

Glatzmaier GA, Roberts PH 1996 Rotation and magnetism of Earth’s inner core Science274:1887–1891

Gubbins D, Bloxham J 1987 Morphology of the geomagnetic field and implications forthe geodynamo Nature (Lond) 325:509–511

Gurnis M 1992 Rapid continental subsidence following initiation and evolution ofsubduction Science 255:1556–1558

Haight RD, Morita RY 1962 Interaction between the parameters of hydrostatic pressureand temperature on aspartase of Escherichia coli J Bacteriol 83:112–120

Hoffman PF 1991 Did the breakup of Laurentia turn Gondwanaland inside-out? Science252:1409–1412

Imshenetsky AA, Lysenko SV, Kazatov GA 1978 Upper boundary of the biosphere ApplEnviron Microbiol 35:1–5

Jannasch HW 1983 Microbial processes at deep sea hydrothermal vents In: Rona PA,Bostrom K, Laubier L, Smith KL Jr, eds Hydrothermal Processes at Sea FloorSpreading Centers New York: Plenum, pp 677–710

Kay M 1955 Sediments and subsidence through time In: Poldervaart A, ed Crust of theEarth: A Symposium Spec Pap 62A New York: Geological Society of America,

pp 665–684

Kearey P, ed 1993 The Encyclopedia of the Solid Earth Sciences Oxford, UK: Blackwell,

p 472

Kerr RA 1995 Earth’s surface may move itself Science 269:1214–1215

Kroener A, Layer PW 1992 Crust formation and plate motion in the Early Archean.Science 256:1405–1411

Kulm LD, Suess E, Moore JC, Carson B, Lewis BT, Ritger SD, Kadko DC, Thornburg

TM, Ebley RW, Rugh WD, Maasoth GJ, Lagseth MG, Cochrane GR, Scamman RL

1986 Oregon subduction zone: Venting, fauna, and carbonates Science 231:561–566.Kuznetsov SI, Ivanov MV, Lyalikova NN 1963 Introduction to Geological Microbiology.English transl New York: McGraw-Hill

Lysenko SV 1979 Microorganisms in the upper atmospheric layers Mikrobiologiya48:1066–1074 (Engl transl 871–877).

Madon M 1992 Mantle In: Nierenberg WA, ed Encyclopedia of Earth System Science,Vol 3 San Diego, CA: Academic Press, pp 85–99

Matthews SW 1973 This changing Earth Natl Geogr 143:1–37

McKenna MC 1972 Possible biological consequences of plate tectonics BioScience22:519–525

Mercy E 1972 Mantle geochemistry In: Fairbridge RW, ed The Encyclopedia ofGeochemistry and Environmental Sciences Encycl Earth Sci Ser, Vol IVA NewYork: Van Nostrand Reinhold, pp 677–683

Morita RY, Haight RD 1962 Malic dehydrogenase activity at 101C under hydrostaticpressure J Bacteriol 83:1341–1346

National Geographic Society 1995 The Earth’s fractured surface (map supplement) NatlGeogr 187(4)

Nierenberg WA 1978 The deep sea drilling project after ten years Am Sci 66:20–29.Palmer AR 1974 Search for the Cambrian world Am Sci 62:216–224

Parkes RJ, Cragg BA, Bale SJ, Getliff JM, Goodman K, Rochelle PA, Fry JC, Weightman

AJ, Harvey SM 1994 Deep bacterial biosphere in Pacific Ocean sediments Nature(Lond) 371:410–413

Paul CK, Hecker B, Commeau R, Freeman-Lynde RP, Neumann C, Corso WP, Golubic S,Hook JE, Sikes E, Curray J 1984 Biological communities at the Florida Escarpmentresemble hydrothermal vent taxa Science 226:965–967

Pedersen K 1993 The deep subterranean biosphere Earth-Sci Rev 34:243–260.Raven PH, Axelrod DI 1972 Plate tectonics and Australian paleogeography Science176:1379–1386

Ritter JRR 1999 Rising through Earth’s mantle Science 286:1865–1866

Ronov AB, Yaroshevsky AA 1972 Earth’s crust and geochemistry In: Fairbridge RW, ed.The Encyclopedia of Geochemistry and Environmental Sciences Encycl Earth Sci Ser,Vol IVA New York: Van Nostrand Reinhold, pp 243–254

Skinner BJ, Porter SC, Botkin DB 1999 The Blue Planet An Introduction to EarthSystem Science 2nd ed New York: Wiley

Smith AG 1992 Plate tectonics and continental drift In: Brown G, Hawkesworth C,Wilson C, eds Understanding the Earth Cambridge, UK: Cambridge Univ Press,

pp 187–203

Straat PA, Woodrow H, Dimmick RL, Chatigny MA 1977 Evidence for incorporation ofthymidine into deoxyribonucleic acid in air-borne bacterial cells Appl EnvironMicrobiol 34:292–296

Strahler N 1976 Principles of Physical Geology New York: Harper and Row

Su W-j, Dziewonski AM, Jeanloz R 1996 Planet within a planet: Rotation of the innercore of Earth Science 274:1883–1887

Szewzyk U, Szewzyk R, Stenstro¨m T-A 1994 Thermophilic, anaerobic bacteria isolatedfrom a deep borehole in granite in Sweden Proc Natl Acad Sci USA 91:1810–1813.Torsvik T, Furness H, Muehlenbachs K, Thorseth IH, Tumyr O 1998 Evidence formicrobial activity at the glass-alteration interface in oceanic basalts Earth Planet SciLett 162:165–176

Tunnicliffe V 1992 Hydrothermal-vent communities Am Sci 80:336–349.

Van Andel TH 1992 Seafloor spreading and plate tectonics In: Brown G, Hawkesworth

C, Wilson C, eds Understanding the Earth Cambridge, UK: Cambridge Univ Press,

pp 167–186

Vine FJ 1970 Spreading of the ocean floor: New evidence Science 154:1405–1415.Wood BJ 1997 Hydrogen: An important constituent of the core? Science 278:1727.Wysession M 1995 The inner workings of the Earth Am Sci 83:134–147