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> I. Prologue

> Chapter 1. Microbial Oceanogr aphy: Roots and Br anches Oceanography

Foundations of Microbial Oceanography , Volume 2, a quarterly 20, Number The O journal of By David M. K arl and Lita M. Proctor

It’s been said, “The farther backwards birth. However, van ,” neither van Leeuwenhoek you look, the farther forward you are improved the art of polishing lenses of nor his contemporaries had any under- likely to see” (Sir Winston Churchill, short focal length, and with a single lens standing of the of these tiny

1874–1965). This is especially true in sci- instrument (“simple” ) he forms. Van Leeuwenhoek was not ceanography S ence where knowledge is cumulative and was able to achieve a magnification of a , and his letters to the Royal contemporary challenges are built on the approximately 275 diameters (Porter, Society about his discoveries have been ociety. C successes of the past. Microbial oceanog- 1976), enough to observe in described as “tiresome because of repeti- raphy is a relatively new discipline that seawater (van Leeuwenhoek, 1677). In a tion and discontinuity” (Kofoid, 1934); opyright 2007 by The O endeavors to establish a comprehensive recent essay on the discovery of micro- he was even called an “immortal dilet- understanding of sea microbes, from , Gest (2004) suggested that tant” (Becking, 1924). It would take to biomes, thereby coupling the credit for the discovery of microbes more than 150 years until the Prussian biosystems to . Microbial should be shared by microscopist Christian Gottfried ceanography S ceanography S oceanography has its historic roots in (1635–1703) and van Leeuwenhoek. Ehrenberg (1795–1876) and others con-

the more established fields of microbiol- Hooke had published a monograph, ducted detailed, laboratory-based inves- ociety. A ogy, oceanography, and marine . , in 1665 showing draw- tigations of , includ- ociety. S ll rights reserved. Permission is reserved. ll rights granted to in teaching copy this and research. for use article R Many current practitioners, however, are ings of microbes that he had seen with ing culture studies of isolated marine end all correspondence to: [email protected] Th e O or unaware of some of the key benchmarks his compound , and includ- microbes. In 1828, Ehrenberg coined and the contributors who helped to ing a section that described—in some the term “bacterium” (from the Greek, establish their discipline. Our introduc- detail—how to construct a microscope meaning “little stick”), and in so doing tion presents a few selected waypoints in from a “very clear piece of Venice .” separated them from other microbes. microbial oceanography. The debate over who should get credit for the discovery of microbes is impor- David M. Karl ([email protected]) is Discovery of Marine tant, but will not be settled here. Rather Professor, Department of Oceanography, Microorganisms than create a revisionist view, we will University of Hawaii, Honolulu, HI, USA. ceanography S The earliest study of marine micro- conclude that van Leeuwenhoek prob- Lita M. Proctor is Associate Research organisms can be traced to a Dutch ably observed, and certainly published, Scientist, University of California, Santa draper and amateur lensmaker, Antony the first description of a “sea microbe.” Cruz, CA, USA, and currently Program ociety, P van Leeuwenhoek (1632–1723). Others The authoritative, indeed majestic, Director, Molecular and Cellular Biosciences, Box 1931, R O Box before him, dating back to Leonardo biography of van Leeuwenhoek by Directorate of Biosciences, National Science da Vinci in the fifteenth century, had C. Dobell (1932), published on the Foundation, Arlington, VA, USA. Opinions, ockville, MD 20849-1931, USA ockville, employed magnifying lenses for the 300th anniversary of van Leeuwenhoek’s findings, and conclusions or recommenda- epublication, systemmatic , study of small objects, and the com- birth, should be required reading for tions expressed in this paper are those of the pound microscope had already been all . authors and do not necessarily reflect the invented before van Leeuwenhoek’s Despite his ability to observe “little views of the NSF. .

16 Oceanography Vol. 20, No. 2 Ehrenberg was also one of the first sci- Golden Age of ,” was the (1856–1953) and the Dutch microbiolo- entists to systematically describe use of pure cultures. This was often gist (1851–1931) led microbes (, , foramin- considered a requirement, for example, to the development of the enrichment ifera, coccolithophorids) in rocks. His in the application of Koch’s postulates1 culture technique. This single advance influential monograph,Mikrogeologie , (Grimes, 2006). in technology facilitated the discovery published in 1854, marked the beginning In his writings, Pasteur discussed the of chemolithoautotrophic of as a scientific dis- importance of the environment in con- (, sulfur, and iron oxidation cipline and was an important precursor trolling and metabolism, and linked to dioxide fixation), nitro- for modern studies in . he expressed great interest in the nascent gen fixation, and sulfate reduction, lead- During the nineteenth century, there were several other noteworthy advances in our understanding of the microbial world that helped to promote investi- gations of marine microbes. First was Microbial oceanography is a relatively the notion that bacteria were actually new discipline that endeavors to establish a diverse assemblage of related organ- isms, which lead to various proposals a comprehensive understanding of sea for classification. The Prussian biolo- microbes, from genomes to biomes, gist Ferdinand Julius Cohn (1828–1898) thereby coupling biosystems to ecosystems. identified several unique groups of bacteria based on morphology, cellular , pigmentation, and growth characteristics; indeed, he has been credited with founding modern micro- field of microbial , but time did ing to a greater understanding of the role biology (Drews, 1999). Cohn was one not permit his full attention to these of microorganisms, especially bacteria, in of the first to conduct detailed labora- matters. At the diamond jubilee meeting global biogeochemical cycles. Beijerinck tory studies of bacterial growth using of the American Society of Microbiology also was one of the first to recognize defined media, and his work helped to in 1974, coined this dichot- “soluble microbes” and coined the term debunk the concept of “spontaneous omy “Pasteur’s dilemma —The road to describe them. He also founded generation” of life by documenting that not taken,” and rhetorically asked where the School of Microbiology, which vegetative cells, but not , were the field of (includ- became an important center for research killed by boiling water (Drews, 1999). ing marine microbial ecology) would and training of the next generation of His achievements became an important be today if Pasteur had selected it as his microbial ecologists. foundation for modern microbiology, primary research thrust. Instead, the dis- along with the more well-known stud- cipline lay relatively dormant (at least in Access to the Sea ies by (1822–1895) and comparison to medical/industrial micro- The other major root of microbial (1843–1910) on infec- biology) for nearly 50 years. Toward the oceanography, namely developments in tious and , vaccina- end of the nineteenth century, inde- oceanography and , can tion, and fermentation. A hallmark of pendent contributions by the Russian be traced back to Kiel and Plymouth this era, sometimes called the “First Sergei Winogradsky with the comprehensive studies of

1 Koch’s postulates are four criteria that need to be satisfied to prove that a causes a disease: the microorganism must found in every case of the disease, the micro- must be isolated from the diseased and grown in pure culture, the same disease must develop when introduced into healthy individuals, and the microorganism must be re-isolated from the new .

Oceanography June 2007 17 marine by mostly European of Microbiology was well underway by Sevastopol Biological Station of the , including Victor Hansen, Karl 1872, there were no systematic attempts Academy of Sciences of the USSR, also Brandt, , Louis Agassiz, to collect or study marine bacteria on the founded in 1872, was dedicated pri- and Anton Dohrn, among others. In the HMS . However, marily to interdisciplinary studies of , the establishment of the by the end of the nineteenth century, the Black Sea. The Kristineberg Marine Navy Hydrographic Office following the beginning with the French microbiolo- Research Station of the Royal Swedish Civil War and the Fish Commission in gist A. Certes (1884), scientists from Academy of Sciences was founded on 1871 provided new opportunities for at- several countries were focusing on the the west coast of Sweden in 1877 to focus on the study of both coastal and offshore marine . This was fol- lowed by establishment of the Plymouth Marine Laboratory in the United in 1888, marine laboratories By the turn of the twentieth century, in Canada (Atlantic Biological Station oceanographic expeditions routinely collected, in St. Andrews, New Brunswick, in enumerated, and analyzed heterotrophic 1899, and the Pacific Biological Station at Nanaimo, British Columbia, in bacteria and other sea microbes. 1908), Germany (Institut und Museum für Meereskunde in 1900), Bermuda (Bermuda Biological Station for Research in 1903), and Monaco (Musée Océanographique de Monaco, created sea observations and sample collection. microbial assemblages in the sea. In and endowed by Albert the First, Prince In December 1872, HMS Challenger, a 1894, German Bernard Fischer of Monaco, in 1906). 2306-ton, steam-assisted British navy published his landmark treatise Die In the United States, several major corvette, departed from Portsmouth, Bakterien des Meeres (Bacteria of the Sea), research and educational facilities England, on a four-year, worldwide which helped to stimulate similar inves- emerged near the turn of the twen- voyage of ocean discovery. This inter- tigations worldwide, leading to modern, tieth century. The Marine Biological disciplinary expedition provided new integrated studies in the discipline of Laboratory at Woods Hole was founded information on all aspects of the ocean microbial oceanography. in 1888, the same year as the Plymouth as an , and most historians In addition to numerous global Marine Laboratory. Other facilities mark the HMS Challenger expedition ocean expeditions, several key marine included Hopkins Marine Station as the beginning of the discipline of laboratories were established worldwide of Stanford University founded in oceanography. Among others, Ernst by the end of the nineteenth century. 1892, Mount Desert Island Biological Haeckel (1834–1919), one of the leading These facilities provided opportunities Laboratory in Maine founded in of this era, made pioneering for sustained observations and con- 1898, Tortugas Marine Biological contributions to our understanding of trolled on isolated marine Laboratory of the Carnegie Institution , especially the microbes and, more importantly, ready of Washington founded in 1902, and distribution, , and access to the open sea. One of the first Coronado Marine Biological Laboratory of , radiolaria, and diatoms. and most famous of these marine sta- of the University of California (UC) at Despite the fact that bacteria had already tions was the Stazione Zoologica Berkeley founded in 1903 (predeces- been observed in numerous marine eco- founded in Naples, Italy, in 1872 by sor of the George H. Scripps Memorial systems and that the First Golden Age German zoologist Anton Dohrn. The Marine Biological Laboratory in 1909,

18 Oceanography Vol. 20, No. 2 Scripps Institution for Biological Economic Importance. This book was streptomycin. This discovery led to an Research in 1912, and, subsequently, the based largely on the initial work of eventual eradication of and Scripps Institution of Oceanography in the U.S. National Academy of Sciences to a Nobel Prize for Physiology/ 1925). There were also Marine Biological Committee on Oceanography (1927– in 1952. Subsequently, in a special vol- Station of the University of Southern 1937). Key themes in Bigelow’s mono- ume of Deep-Sea Research dedicated California founded in 1911, San Juan graph included: (1) oceanography is to Henry Bryant Bigelow on the occa- Islands Biological Station founded in impossible unless one goes to sea— sion of the twenty-fifth anniversary 1904 (predecessor of the Oceanographic observations are fundamental to under- of the founding of WHOI, Waksman Laboratories, University of Washington, standing, (2) technology drives oppor- (1955) recounted his early studies in 1920); Chesapeake Biological Laboratory tunity and facilitates the creation of new marine . Besides his labo- of the University of Maryland founded knowledge, and (3) the need to shift ratory work, Waksman also attempted in 1920, and Woods Hole Oceanographic research from a descriptive approach to some open ocean fieldwork, which he Institution founded in 1930. an analytical/quantitative one, including characterized as a complete failure. mathematical modeling. These are still “Under the threefold movements of Emergence of Microbial valid guiding principles for contempo- the ship, I immediately became seasick Oceanography rary microbial oceanography. Bigelow and had to leave the work largely to one By the turn of the twentieth century, also concluded that our knowledge of of the assistants who always accom- oceanographic expeditions routinely col- bacteria is “woefully scant” and empha- panied me. After two valiant efforts to lected, enumerated, and analyzed hetero- sized that they must be studied to under- carry out studies on the moving boat, trophic bacteria and other sea microbes. stand the organic fertility of the sea. He I made no further attempts.” Bigelow’s A fundamental scientific question dur- also suggested that the process of nitro- comment, “ was wasted on him,” ing these early studies was whether gen (N2) fixation, already reported in was entirely appropriate. there existed truly “marine” bacteria many terrestrial habitats since its discov- Across the United States, two addi- that could be distinguished from their ery in the early 1900s, should also occur tional laboratories, one at Stanford terrestrial and freshwater counterparts. in the sea. It would take another three University’s Hopkins Marine Station Because most bacteria originally isolated decades before Richard Dugdale and his in Pacific Grove, California, and the from nonmarine sources were unable colleagues reported N2 fixation in the other in San Diego, California, at to survive for extended periods when Sargasso Sea (Dugdale et al., 1961). Scripps Institution of Oceanography inoculated into seawater, a focus of this Perhaps the greatest contribution that (SIO), were beginning to conduct inde- research on the nature of marine bacte- Bigelow made to microbial oceanogra- pendent studies on sea microbes. At ria was on a diagnostic salt requirement phy was to recruit Selman A. Waksman, a Hopkins, these were organized and led or salt tolerance. The existence of marine well-established microbiologist from by Cornelis B. van Niel (1897–1985), a bacteria remained an open question Rutgers University, to Woods Hole to distinguished scientist from the Delft until the early 1960s when a Na+ require- begin a new program in marine microbi- School of general microbiology. In ment for growth was discovered as a ology. Waksman joined the WHOI staff addition to many important contribu- unique characteristic of marine bacteria in 1931 and made several fundamental tions including his pioneering work (MacLeod, 1985). contributions over the next few years, on bacterial and the In 1931, Henry Bryant Bigelow especially on the process of organic mat- metabolism of sulfur bacteria, van Niel (1879–1967), the inaugural director ter and on the marine made a lasting contribution by organiz- of the newly established Woods Hole cycle. In 1939, he returned to ing and teaching a summer course at Oceanographic Institution (WHOI), his “roots,” , and within Hopkins. Over the next three decades, published his benchmark monograph a decade had isolated and character- this served as an important training Oceanography: Its Scope, Problems, and ized 10 compounds, including ground for many future marine micro-

Oceanography June 2007 19 biologists (Spath, 2004). At SIO, Haldane ods had been introduced for micro- interactions, respectively. Unfortunately, Gee was appointed assistant professor bial- enumeration and estimation of when their core funding from the U.S. of bacteriology in 1928. Others before respiration, metabolism, or Atomic Energy Commission (pre- him, including Charles Kofoid (proto- growth. In 1963, the Institute of Marine decessor of the Energy Research and zoa) and Winfred Allen (diatoms and Resources at SIO established the Food Development Agency and, subsequently, ), had studied eukaryotic Chain Research Group (FCRG). This the Department of Energy) dried up, the microorganisms, but Gee was the first to group was founded and led by John FCRG dissolved, although the individual specialize in bacteria. D.H. Strickland, an analytical chem- scientists continued to make pioneer- At the thirty-first meeting of the ist by training, born and educated in ing contributions, especially in the area Society of American the United Kingdom. In 1952, he emi- of marine microbial ecology. During (predecessor of the American Society grated to Canada and worked at the this same period, circa 1960–1980, other for Microbiology), December 30, 1929, University of British Columbia and at scientists worldwide began making fun- to January 1, 1930, Gee described a new the Fisheries Research Board of Canada damental contributions regarding the bacteriological sampler for use in deep at Nanaimo, British Columbia, before biology and ecology of sea microbes. By water. He also reported preliminary data moving to Scripps. At Nanaimo he began the early 1970s, most marine science/ for total bacterial counts from several a long-term collaboration with Tim oceanography departments, and many surveys off southern California. He con- Parsons, and in 1968 they published departments of microbiology/bacteriol- cluded that “significant counts in the the first edition of their classic mono- ogy/environmental science had at least water are restricted to the topmost 25 m, graph, Handbook of Seawater Analysis one “marine microbiologist” on staff. below which there is apparent sterility (Strickland and Parsons, 1968). As leader This led to rapid growth in training and until the bottom zone is reached” (Gee, of the FCRG, Strickland assembled an of new scientists into the 1930a). That same year, Gee (1930b) outstanding, interdisciplinary scientific collective workforce of this challenging reported on the status of marine bac- staff, including Angelo Carlucci (bac- and expanding discipline. Ironically, very teriology at the fourth Pacific Science teria), Richard Eppley (phytoplank- few universities offer advanced degrees Congress in Java. Based on a compilation ton), John (), Osmund in marine microbiology (or marine of 136 scientific papers on the subject, Holm-Hansen ( and bio- microbial ecology or microbial ocean- he concluded that, “Much of this work chemistry), Peter Williams (organic ography). The International Max Planck must be regarded as incomplete and biogeochemistry), and Michael Mullin Research School of Marine Microbiology some of it can be discarded entirely in (mesozooplankton). Collectively, this (MPI-MM), a joint program between view of developments in bacteriology in team developed new methods, promoted the MPI-MM in Bremen, the University the past 10 years.” He went on to state, systematic studies of trophic of Bremen, The Alfred Wegener Institute “The first prerequisite for a general sur- and interactions with an emphasis on for Polar and Marine Research (AWI), vey is the development of special meth- pelagic marine ecosystems, and trained and the International University of ods.” Unfortunately, Gee’s career was cut a large number of students and postdoc- Bremen (IUB) is the best and, perhaps short due to illness and he left SIO in toral scholars that helped to continue only, contemporary example. 1932 (Yayanos, 2003). Gee was replaced the tradition. After Strickland’s death by Claude E. ZoBell, who worked tire- in 1970, the FCRG sustained interdis- ZoBell’s Marine Microbiology lessly for the next five decades to help ciplinary research in microbial bio- and Related Works establish and promote the discipline. The geochemistry under shared leadership. Claude E. ZoBell (1904–1989) began publication of his monograph, Marine Farooq Azam and George Jackson were his training in Microbiology, is cited by many as the added to the staff to further enhance at the Hooper Foundation for Medical beginning of a new era (see below). leadership in microbial food webs and Research at the University of California, By the early 1960s, many new meth- food-web modeling/physical-biological Berkeley. His Ph.D. research, com-

20 Oceanography Vol. 20, No. 2 pleted in 1931, was on the growth and less inclusive than the title, Marine and are dealt with in seven pages; metabolism of Brucella. In 1932, he Microbiology, implied because it focused beyond the re-iterated statement that moved to the “temporary” position of almost exclusively on marine bacteria the is largely responsible instructor in marine microbiology at and not “microbes” in a more general for the production of organic matter in Scripps Institution of Oceanography, sense of the term. In fact, the main title the ocean, the are not mentioned; where he remained active until approxi- Marine Microbiology and the subtitle nor are the protozoa.” Van Niel ended mately 18 months before his death in A Monograph on Hydrobacteriology are his review by stating, “as a monograph it 1989. According to published records, ZoBell’s initial responsibility was “to determine the extent to which bacte- ria are active in the open ocean and to assess their possible importance as geo- ...the foundation of our discipline chemical agents” (Yayanos, 2003). While continues to expand with new fundamental significant progress has been made in the intervening 75 years, these themes knowledge about life in the sea. remain as the contemporary challenges of microbial oceanography, collec- tively comprising the “Second Golden Age of Microbiology.” somewhat contradictory, because the does not reach a very high standard, and In 1946, ZoBell published his now former implies all marine microbes seems, on the whole, rather trifling.” classic book Marine Microbiology: A (including bacteria, and fungi, Despite those contemporary criti- Monograph on Hydrobacteriology. Many algae, and ), while the latter cov- cisms, ZoBell’s collective contribu- science historians consider this to be ers only bacteria but includes all aquatic tions, including his monograph Marine the modern beginning of the discipline; (marine, freshwater, estuarine, ground- Microbiology, a significant bench- Donald McGraw recently character- water, wastewater) environments. This mark in the history of microbial ocean- ized ZoBell’s magnum opus as a pio- important point on the relatively narrow ography. ZoBell was only 42 years old neering “manifesto” in the founding of scope of the monograph relative to the when his monograph was published; he marine microbiology (McGraw, 2006). potential scope of the discipline itself, went on to publish nearly 300 scientific Although others before him had written despite the broad title, was echoed by papers on various aspects of marine scholarly monographs on sea microbes, van Niel, a recognized leader in general microbiology, , and ZoBell’s was the first that was written by microbiology at that time. In a book petroleum microbiology, and to par- a “twentieth century scientist” (he was review that appeared in The Quarterly ticipate in many important research born in Utah just after the turn of the Review of Biology, van Niel (1946) stated, expeditions during his career. For century), and his monograph reviews “This preference on the part of ZoBell is example, during the Danish Galathea the many key discoveries that had taken hardly an adequate reason for the use of deep-sea expedition (1950–1952) led by place in the decades since the mono- a title which suggests an account of the Anton Bruun, ZoBell was able to docu- graphs by Fischer (1894) and Benecke nature and activities of marine microor- ment bacterial life at the bottom of the (1933) had been published. However, ganisms. Instead, the contents are almost 10,462-m-deep Philippine Trench. He not everyone was uniformly pleased with exclusively limited to a rather elemen- also demonstrated a growth preference the scope and quality of ZoBell’s mono- tary treatise of the bacterial population in these populations for low temperature graph. A book review that appeared in of the ocean, with a few brief sections (2.5°C) and high pressure (1000 atm), Ecology (Burrows, 1946) was critical on bacteria in marine air, in , and conditions that were uniquely charac- of the fact that the volume was much in salt- and freshwater lakes. The yeasts teristic of their native habitats (ZoBell,

Oceanography June 2007 21 1952). Donald McGraw has written monograph also includes a comprehen- were actually microorganisms at all, extensively about ZoBell and his impact sive summary of the Russian research but rather body parts of larger marine on marine microbiology (McGraw 2001, effort in marine microbiology, and a organisms. A second monograph 2004, 2006), and four mini-biographies bibliography of more than 400 Russian by A.E. Kriss and others, Microbial on various aspects of ZoBell’s scientific papers. The bulk of the 536-page vol- Population of Oceans and Seas, also writ- career appeared in the Proceedings of the ume summarized the “quantitative ten in Russian, was later translated into 8th International Symposium on Microbial distribution of heterotrophic micro- English by K. Syers, edited by G.E. Fogg, Ecology (e.g., see Lappin-Scott, 1999). In organisms throughout the seas and and published in 1967. 1985, a festschrift of the Geomicrobiology oceans,” including bacteria and yeasts, In 1965, P. Gray and J.D. McCarthy initiated a new publication , Modern Biological Studies. The idea was to commission scholarly monographs It is remarkable how rapidly on various topics that were identified by them to be timely and important. our paradigms are shifting... For Volume 1 of this series, they turned to E.J. Ferguson Wood (1904–1972), then professor of marine microbiol- ogy at the Institute of Marine Sciences Journal was dedicated to ZoBell, who was using a of different methods of at the University of Miami (predeces- the journal’s founder and editor-in-chief enumeration, complete with numer- sor of the Rosensteil School of Marine (Morita, 1985). ous tables and figures, and an exhaus- and Atmospheric Sciences) to prepare It was quite a while before another tive description of many of the a synthesis entitled Marine Microbial major synthesis of research in marine that were isolated. Typically, fewer than Ecology. Wood, an Australian-born and microbiology was undertaken in the 100 bacterial cells per milliliter (and -educated began his career form of a monograph. In 1955, Jean often, zero) were reported for growth as a marine scientist studying fish spoil- Brisou’s La Microbiologie du Milieu on various media, compared to orders age and the biology of sea grasses, later Marin was published, but to our knowl- of magnitude greater cell abundances moving into studies of marine phyto- edge this work was never translated into derived from direct microscopic exami- plankton. After a successful, 30-year English and, therefore, it had compara- nation of seawater samples concentrated career at the Commonwealth Scientific tively minor impact on the field as a on membrane filters. Jannasch and Jones and Industrial Research Organization whole. A.E. Kriss completed the Russian (1959) also discussed this method- (CSIRO), he moved to the University of version of Marine Microbiology (Deep ological mismatch, and even the direct Miami in 1963 where he worked until Sea) that the Academy of Sciences, microscopic methods using membrane his return to Australia in 1970. His con- USSR, published in 1959; a year filters systematically underestimated the tributions, especially as a prolific scholar later it was awarded the Lenin Prize. true abundance of marine bacteria. One and author in the last decade of his life, J.M. Shewan and Z. Kabata subsequently of the more bizarre aspects of Kriss’s established him as one of the leaders translated this book into English, and work is his report of strange and mor- of his generation. In the preface to his Oliver & Boyd published it under the phologically complex “microbial forms” monograph, Wood stated, “In marine same title (Kriss, 1963). According to in many samples that were observed microbiology our facts are so discrete ZoBell’s review, the English under the microscope. These unusual and disconnected that they do not form has some new material not found in “microbes” (called Krassilnikoviae a story, and the most important truths either the original Russian or previous [ZoBell, 1963]) were never cultured, of our discipline are still unknown.” German version (ZoBell, 1963). The and it now seems highly unlikely they He went on to conclude that “we now

22 Oceanography Vol. 20, No. 2 need breadth and vision rather than habitats, Microbial Seascapes, which research results and discuss problems of specialists … (people) who can inte- helped to illuminate the microbial world mutual concern” (Oppenheimer, 1963). grate rather than dissect.” Although he (Sieburth, 1975). Apparently, he was either unaware of the was one of ZoBell’s close colleagues, 1957 symposium in Dunedin, or didn’t Wood pointed out that ZoBell’s book Symposia, Edited Volumes, think much of it! In any case, the 1961 Marine Microbiology was rather narrowly and the Proliferation of ASM symposium was a much larger, focused on bacteria and also felt that Trade Journals more comprehensive event attended by the terms “microbiology” and “bacteri- As scientific disciplines develop and a veritable who-was-who in the disci- ology” were often used synonymously mature, they leave an archival legacy of pline at that time. The published volume and therefore incorrectly. He called for new information. Oftentimes, mono- contains 66 chapters divided into seven an integrated study of the ocean as an graphs do not adequately capture the sections: (1) introduction—5 chapters; ecosystem. Wood published a second details and, sometimes, subtle impli- (2) the producers and their relation to monograph, Microbiology of Oceans and cations of all advances in methodol- the chemical and biological environ- , just two years later, and he ogy and concept. Special symposia, key ment—9 chapters; (3) geomicrobio- served as founding co-editor of the series review articles, and original refereed logical activities of marine microorgan- Advances in Microbiology of the Sea in publications are the primary vehicles isms—7 chapters, (4) ecology of algae, 1968 (see next section). His contribu- for advancing the state of knowledge. In protozoa, fungi, and viruses—14 chap- tions were indeed significant. 1957, a special symposium on “Marine ters; (5) heterotrophy in marine microbi- In 1972, Rita Colwell and Michael Microbiology” was held in conjunction ology—10 chapters; (6) distribution and Zambruski prepared a translated, edited, with the thirty-second meeting of the of marine bacteria—14 chap- and revised version of A.G. Rodina’s Australian and New Zealand Association ters; and (7) marine bacteriology and the monograph on Methods in Aquatic for the Advancement of Science at problem of mineralization—7 chapters. Microbiology, which had last appeared Dunedin, New Zealand. T. M. Skerman If a symposium were to be organized in Russian in 1965. Because the expand- compiled the proceedings of this inter- today, many of these sections from the ing discipline of marine microbiology national symposium and published 1961 event would align with contem- was still very much methods limited them in 1959 as Contributions to Marine porary issues and challenges, which is at that time, the introduction of novel Microbiology (Skerman, 1959). This pub- somewhat sobering to contemplate given methods and instrumentation—some lication included a broad range of papers the enormous progress that we have known only to those working in by C.E. ZoBell, D.J. Rochford, V.B.D. achieved during the past four decades. Russia—was invaluable. Skerman, E.J. Ferguson Wood/P.S. Davis, In chapter 48 of the symposium volume, During the next three decades and L.G.M. Bass Becking. A.E. Kriss discusses “The immediate (1976–present), several additional A few years later, C.H. Oppenheimer tasks of marine microbiology.” He lists monographs on aquatic microbiology/ compiled and edited a series of papers four challenges: (1) extension of at-sea marine microbiology have appeared, based on a special “Symposium on observations and integration of marine including Sieburth (1979), Rheinheimer Marine Microbiology” that was held in microbiology into “mainstream” ocean- (1980), Austin (1988), Sorokin (1999), conjunction with the sixty-first annual ography, especially marine geochemis- and Munn (2004). All serious practitio- meeting of the American Society of try; (2) initiation of year-round, repeat ners and apprentices should read these Microbiology (ASM) in April 1961. In observations to resolve daily, seasonal, works, cover to cover, to gain an appre- the preface to the volume, Oppenheimer and interannual variations in micro- ciation for the origin and of states that this symposium was the “first bial population structure and processes; ideas in the discipline. John Sieburth attempt to bring together the leading (3) estimation of primary productiv- also prepared a wonderful pictorial essay investigators in this field from all parts ity and determination of production: on marine microorganisms and their of the world to exchange ideas, present ratios; and (4) initiation of a

Oceanography June 2007 23 systematic study of , Among several other provocative state- ended in 1985 with volume 3, edited by especially in the deep sea. These “tasks” ments, he concluded that “so many H.W. Jannasch and P.J. leB. Williams. are all still relevant today; we apparently recent discoveries cast doubt on - In his review of Advances in Aquatic have some work to do. ries which seemed to be solidly founded Microbiology volume 1, Tom Brock Other key symposia were orga- that the reviewer finds it hard to give a expressed doubt about the long-term nized to bring international research- factual evaluation,” but that “valuable success of “one more review series in ers with a common interest in sea information on all subjects is coming microbial ecology.” Unfortunately, Brock microbes together to exchange data, to hand.” Therefore, “it seems high time was right on with this assertion, and the knowledge, and their plans for future for marine microbiologists to sum up series was eventually terminated. When research. Rita Colwell, Richard Morita, the work that has been done, consider asked about the demise of this important and others were instrumental in the how they can fill the gaps in existing publication, volume 3 editor Williams organization of two U.S.-Japan confer- studies and proceed to solve what may noted that the series was perceived by ences on marine microbiology. The be of global importance, the true role some to be in with others in first was held in Tokyo in 1966, and the of microorganisms in the oceans, seas the growing field of microbial ecology, second was held at the University of and estuaries of the world.” Amen! This and that it required the full-time atten- Maryland in 1972 (Colwell and Morita, volume also contained eight scholarly tion of one or more editors to sustain 1974). Edited symposia proceedings review articles on subjects ranging from it (personal communication to DMK, also included Stevenson and Colwell the kinetics of phytoplankton growth February 2007). (1973) and Colwell and Foster (1979). (R. Eppley and J.D.H. Strickland), to Other edited volumes have also In 1962, Samuel Meyers of Louisiana numerical taxonomy of marine bacteria appeared since the publication of State University initiated the Aquatic (W. Hodgkiss and J.M. Shewan), to the ZoBell’s monograph. In 1976, Carol Microbiology Newsletter, which he edited, distribution and ecology of marine yeasts D. Litchfield, then a professor at Rutgers printed, and distributed for more than (N. van Uden and J.W. Fell). By the end University, edited a volume entitled four decades. The newsletter covered a of this 239-page work, most readers were Marine Microbiology, as the eleventh broad range of topics, including reports already looking forward to volume 2; book in the Benchmark Papers in of meetings and related activities of unfortunately, it never appeared. Microbiology series. This volume was mutual interest. When Meyers retired, so The series was reincarnated nearly comprehensive in scope and included too did the Newsletter, unfortunately. a decade later as volume 1 of Advances annotations by Litchfield on the sig- With great expressed need, a new con- in Aquatic Microbiology edited by nificance of each benchmark paper that tributed series, Advances in Microbiology M.R. Droop and H.W. Jannasch (1977). she had selected for presentation. Other of the Sea, edited by M.R. Droop and The scope was broadened to include works edited by Sleigh (1987), Ford E.J. Ferguson Wood appeared in 1968 studies of both marine and freshwater (1993), Cooksey (1998), and Kirchman (Droop and Wood, 1968). The scope ecosystems, from microbial physiology (2000), and two comprehensive aquatic/ was summarized in the preface by to ecology, with a stated goal of identi- marine microbiology methods manuals M.R. Droop: “In so far as it can be con- fying common ground across aquatic edited by Kemp et al. (1993) and Paul sidered a corporate science, . Unlike some other “Advances (2001), have also appeared during the microbiology may be defined as the in…” series, this one was not intended to past two decades. Ironically, Kirchman’s study of marine processes effected by be an annual publication, and volume 2 Microbial Ecology of the Oceans (2000, microorganisms. This, of course, includes did not appear until 1980 (also edited second edition due in 2007) had an the study of the agents themselves.” by M.R. Droop and H.W. Jannasch). acknowledged and deliberate focus on In Chapter 1, “Perspectives in Marine Despite the growing importance of heterotrophic bacteria in the upper Microbiology,” E.J. Ferguson Wood pro- aquatic microbiology, especially marine euphotic zone, so it does not provide vided a status report of the discipline. microbiology, the publication series a comprehensive coverage of the disci-

24 Oceanography Vol. 20, No. 2 pline. In this regard, it is a flashback to and enjoyable. There was an element of review? These are new, twenty-first cen- the criticism that van Niel and others excitement being among the first to scan tury challenges for our discipline and for voiced when ZoBell’s book was first pub- the current issue of your favorite peri- science as a whole. lished in 1946. Probably no book, edited odical, to read about the latest discov- series, or monograph will ever be com- ery or contribution. One of us (DMK) Technology, Discovery, plete, given the breadth and scope of the remembers attending a seminar, circa and Shifting Paradigms modern discipline of microbial oceanog- 1975, by marine ecologist Joel Hedgpeth The field of microbial oceanography is raphy, so compromises must be made. who argued that the invention of the currently methods, data, and knowledge When ZoBell published his mono- photocopy machine was one of the worst limited. As new methods, instruments, or graph in 1946, the journals Applied things that had happened to the dissemi- technologies are introduced, novel data and Environmental Microbiology, nation of scientific information, because sets are obtained about microbial life in Aquatic Microbial Ecology, Biological students started photocopying, rather the sea, which leads to an improvement Oceanography, Deep-Sea Research, than carefully and critically reading, in understanding and the development Ecosystems, Environmental Microbiology, the scientific literature. Today we have of improved paradigms and models Geomicrobiology, Journal of Plankton even more rapid Internet-based infor- (Doney et al., 2004; Rothstein et al., Research, and Oceanography, mation exchange, and scientific papers 2006). This interplay of theory, engineer- Marine Biology, Marine Ecology Progress are downloaded in digital format and ing, and scientific application continues Series, Microbial Ecology, and others that stored electronically, but oftentimes still to define progress in our discipline. currently publish most of the original not carefully or critically read. Carlos Space limitations preclude a detailed papers on sea microbes did not exist. Duarte (professor of marine sciences and accounting of the many significant tech- There were fewer scientists overall, and president-elect of the American Society nology-driven advances in the field of the accumulation rate of new knowl- of Limnology and Oceanography) esti- microbial oceanography in the past few edge was manageable. Today, we have mated in a personal communication that decades, but we itemize a few here to more scientists, more journals, and more approximately 3000 papers are published serve as examples: (1) the discovery of a long-lived radioactive isotope of car- bon, carbon-14 (Ruben and Kamen, 1940), that led to novel methodolo- gies for measurements of oceanic pri- ...we may not yet be in a position to mary production (Steemann Nielsen, provide an ecumenical account of 1951) and heterotrophic bacterial even the most basic processes of carbon production (Parsons and Strickland, 1962); (2) the invention of the “plastics- and through marine systems. irradiated-etched” (PIE, later known by the trade name Nuclepore) membrane filters (Fleischer et al., 1964) that enabled routine, accurate estimation of marine information that needs to be carefully each year in the field of marine micro- bacterial abundance by epifluorescence sorted and assimilated. In the “good old bial ecology, and that number will only (Hobbie et al., 1977) and to days,” all scientists routinely spent sig- increase in the future. How do we deal the discovery of the “widespread occur- nificant amounts of their time, usually with this avalanche of new knowledge? rence of a unicellular, marine, planktonic between laboratory experiments or field And how can the field as a whole main- cyanobacterium” belonging to the expeditions, reading books and journals tain a high standard if there is an expo- (Waterbury et al., 1979), in the library. This was both necessary nential increase in the burden for peer the second most abundant

Oceanography June 2007 25 in the sea; (3) the application of satel- Acknowledgements Marcel A. Gradsten and Carol D. Litchfield). Pp. 8–10 in Marine Microbiology. C.D. Litchfield, lite-based remote sensing of ocean color We are indebted to all those who have ed., Dowden, Hutchinson & Ross, Inc., (Smith and Baker, 1982), which led to made contributions to our discipline, Stroudsburg, Pennsylvania. synoptic global maps of near-surface both at sea and in their shore-based Chisholm, S.W., R.J. Olson, E.R. Zettler, R. Goericke, J.B. Waterbury, and N.A. and estimates of total oce- laboratories, that collectively form the Welschmeyer. 1988. A novel free-living prochlo- anic (Behrenfeld basis for our contemporary understand- rophyte abundant in the oceanic euphotic zone. and Falkowski, 1997); and (4) the transi- ing of sea microbes. DMK would like to Nature 334:340–343. Colwell, R.R., and J. Foster, eds. 1979. Aquatic tion of laser-based and thank Professor Art Yayanos for help- Microbial Ecology, Proceedings of the confer- cell-sorting techniques from the medical ful discussions and relevant historical ence sponsored by the American Society for Microbiology, 7–10 February, 1979, Clearwater laboratory to the ocean research vessel information. We also wish to thank the Beach, Florida, Maryland Sea Grant, College (Yentsch et al., 1983) that led to the dis- Gordon and Betty Moore Foundation Park, MD, 460 pp. covery of , the most abun- and the Agouron Institute for their lead- Colwell, R.R., and R.Y. Morita, eds. 1974. Effect of the Ocean Environment on Microbial Activities. dant phototroph in the sea (Chisholm ership in and generous support of the University Park Press, Baltimore, MD, 587 pp. et al., 1988). These are just a few of the field of marine microbiology, and the Cooksey, K.E., ed. 1998. Molecular Approaches many examples of how technology drives U.S. National Science Foundation for sig- to the Study of the Ocean. Chapman & Hall, London, 549 pp. discovery in the field of microbial ocean- nificant investments, including but not DeLong, E.F., and D.M. Karl. 2005. Genomic per- ography. Without an accurate inventory limited to the recent establishment of spectives in microbial oceanography. Nature 437:336–342. and basic ecological understanding of the Center for Microbial Oceanography: Dobell, C. 1932. Antony van Leeuwenhoek and his the dominant groups of sea microbes, we Research and Education (C-MORE) at “Little .” Harcourt, Brace and Company, cannot yet claim to have achieved success, the University of Hawaii. NY, 435 pp. Doney, S.C., M.R. Abbott, J.J. Cullen, D.M. Karl, though we have made great progress. and L. Rothstein. 2004. From to ecosys- REFERENCES tems: The ocean’s new frontier. Frontiers in Ecology and the Environment 2:457–466. Epilogue Austin, B. 1988. 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