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Biographical Memoirs: Volume 81

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Biographical Memoirs: Volume 81 MARVIN P. BRYANT July 4, 1925–October 16, 2000 BY ARNOLD L. DEMAIN AND RALPH F. WOLFE MARVIN P. BRYANT, EMERITUS professor of microbiology at the University of Illinois, died on October 16, 2000, at his home in Savoy. Illinois, at the age of 75. Marv was born on July 4, 1925, to Melvin Berry and Emna Louise Bucklin Bryant. He was raised on the edge of the foothills in Boise, Idaho, with summer and fall excursions to the family ranch next to the primitive area of the Middlefork of the Salmon River. The environment provided by the area, especially the associations with horses and various ruminants, the freedom and support he received from his parents, and his natural inclination toward biology directed him toward his then unknown goal of doing research in rumen microbiology. After serving in the U.S. Air Corps during World War II he vowed in 1945 that he would never leave the mountain area, and he completed his diploma at Boise Junior College. In 1946 Marv married Margaret Amelia Betebenna. He started in forestry and switched to soils. Counseling by botany professor Donald Obee moved him into bacteriology and propelled him toward Washington State College in Pullman. According to Marv, his reticence to meet the public and his belief that research and publications alone would

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Biographical Memoirs: Volume 81 largely satisfy his goals helped to move him toward a career in research. THE PULLMAN YEARS In three short years, the general theme of his life’s work was set. As a new student with junior standing and with a wife and three-month-old daughter to support, he needed to supplement his GI Bill funds with part-time labor. His first official contact was with Professor Robert E. Hungate, the father of rumen microbiology research and anaerobic microbiology. Hungate was a scientific descendent of the Delft school of microbiology (Biejerinck → Kluyver → van Niel) and was the latter’s first American Ph.D. student. Marv started working in Hungate’s lab as the glassware washer during the daytime and was later switched to lab work, expediting the research of Hungate and of his Ph.D. student, R. H. McBee. This work was a revelation and better than any possible formal course. The poor funding of research outside of agriculture in this early postwar period made it necessary for Hungate and McBee to make essentially all of their glass apparatus by hand from such materials as Pyrex culture tubes, Erlenmeyer flasks, Kjeldahl flasks, glass tubing, and assorted salvage. Among the things “manufactured” were a complete Warburg apparatus, micro-modification of the Newcomer-Haldane constant pressure volumetric gas analyzer, all condensers, and various units required for the determination of lactate and volatile fatty acids when chromatographic and enzymatic methods were just beginning to evolve. Among Marv’s duties were maintenance of a few stock cultures including the important thermophilic cellulolytic species, Clostridium thermocellum; determination of fermentation end products and fermentation balances of various anaerobic species; enumeration and isolation of anaerobic

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Biographical Memoirs: Volume 81 soil cellulolytic bacteria, Ruminococcus albus; and the first isolation of the “less actively cellulolytic rod” later named Butyrivibrio fibrisolvens. In association with the General Electric Research Laboratory in Schenectady, N.Y., Hungate outlined experiments in which Marv did in vitro rumen fermentations of wood treated with cathode rays. Results showed that the cellulosic fraction of wood was released from lignin and made available to anaerobic microbial digestion and volatile acid production, while the lignin remained indigestible at certain radiation dosages. In June of 1949 he received his B.S. degree, and Hungate, having acquired funds for research from state liquor tax money, placed Marv on a half-time research assistantship at a salary of about $1,500 a year. His research involved the isolation and characterization of the small rumen spirochete of the genus Treponema, which could move through agar or particulate forage and compete with cellulolytic bacteria for use of the soluble sugar energy sources produced by the latter from cellulose. The report of his research was the first published work on fermentation products of a spirochete and suggested strong metabolic interactions between cellulolytic and noncellulolytic fermentative bacteria in anaerobic ecosystems, a finding that only later received extensive documentation. Electron micrographs of the aging cells taken with the aid of a physics graduate student showed the periplasmic membrane and fibrils and protoplasmic cylinder of spirochetes, but these were not recognized until much later. Because Marv wanted to continue on to his Ph.D. at Pullman and Hungate believed that he needed more interactions with course work and research in another area of the country, Marv continued his assistantship through Washington State College for an eight-month period in 1949 at Cornell University. During this period he took course work

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Biographical Memoirs: Volume 81 in animal nutrition, bacterial metabolism, industrial microbiology, and bacterial cytology. He also had a large number of associations with other professors and students in both veterinary medicine and bacteriology. These included H. H. Dukes, professor of veterinary physiology; James M. Sherman, professor of bacteriology and long-time editor of the Journal of Bacteriology; and Meyer J. (“Mike”) Wolin, then an undergraduate student. Marv’s research was conducted in association with Professor Robert Dougherty on the microbiology and physiology of acute indigestion, lacticacidosis, in sheep. Streptococcus bovis was found to be the initiator of high rumen lactate and was often followed by members of the genus Lactobacillus. During his stay in Ithaca, Professor William Pounden of Ohio State University visited and carried word to Beltsville Agricultural Research Center that Hungate had a graduate student working in rumen microbiology. A research bacteriology position was offered by the Bureau of Dairy Industry and, after a strong push from Hungate, Marv decided to accept. THE BELTSVILLE YEARS Having received his M.S. degree in 1950 from Washington State College, Marv was concerned about completing his Ph.D. degree and this was made possible at his own expense and time by Lane A. Moore, head of the dairy cattle nutrition group at Beltsville, and Professor Raymond Doetsch, Department of Microbiology, University of Maryland, College Park, just a short distance from Beltsville. He was allowed to take one course per semester at College Park and his thesis research was completed while still working at Beltsville. He received his Ph.D. degree from the University of Maryland in 1955. Marv’s faith in his ability to adequately advance basic

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Biographical Memoirs: Volume 81 knowledge on rumen microbiology was very low, and during the first few years at Beltsville he very much missed Hungate’s guidance. He was given essentially complete freedom to work within the huge area of rumen microbiology by Moore, who was an outstanding nutrition expert and research administrator, but who could offer essentially no guidance in microbiology. Marv’s main goals were to taxonomically describe, with emphasis on ecologically important metabolic features, the numerous species of rumen bacteria and to chemically identify “unusual” growth factors present in rumen fluid but not in most organically rich growth media. Hungate had worked mainly with pure cultures of the cellulolytic population and his development of classic anaerobic techniques and habitat-stimulating growth media had largely removed the blocks confronting further advances in isolation and description of rumen bacteria. However, Hungate was already beginning to feel that kinetic studies of major overall rumen biochemical reactions were more important to his research effort. In addition, Doetsch was formulating the idea that the “physiological” approach using washed suspensions of mixed rumen microorganisms would probably yield the most fruitful results in the future. There were thus major currents against Marv’s emphasis on pure culture studies, but he continued this emphasis with apprehension. During Marv’s early research, the general field of anaerobic bacteriology remained in a chaotic state because of a general lack of knowledge about anaerobic bacteria, the failure of most workers to determine catabolic products of energy metabolism, and the inability of most microbiologists to grow and isolate the relevant species. Techniques such as determination of taxonomically important cellular constituents, percent guanine plus cytosine in the DNA, and DNA-DNA hybridization were for the most part yet to

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Biographical Memoirs: Volume 81 be developed. Even with the development of these methods and various others, many problems of relatedness among major microbial taxonomic groups still existed. When his work at Beltsville was initiated, the only rumen anaerobes that had been studied and named with enough detail for other workers to identify were the cellulolytic species, Bacteroides succinogenes by Hungate and Ruminococcus flavefaciens by Sijpesteijn. Hungate had published on various Ruminococcus species and B. succinogenes earlier but had not named them, and Sijpesteijn’s work at Delft had been delayed for several years by the German invasion of Holland. Marv’s first concern was to develop and evaluate methods for enumerating and isolating the more numerous bacterial species. The anaerobic roll-tube methods of Hungate were somewhat modified for larger scale studies. The 40 percent rumen fluid-glucose-cellulose agar roll tube (RGCA) medium with CO2 gas phase, bicarbonate as the main buffer, and cysteine as added reducing agent was a slight modification of Hungate’s selective cellulose agar medium and allowed the isolation of most of the predominant carbohydrate fermenting species. Traces of O2 were removed from the commercial gases that were passed through a glass column containing hot copper filings. This column turned dark as the copper oxidized and could be quickly reduced by exposure to H2. A balanced mineral anaerobic solution similar to the growth medium, but with rumen fluid and sugar energy sources removed, served as the rumen fluid diluent. Large numbers of bacterial strains were rapidly isolated by picking colonies from large-diameter (18 mm) roll tubes with platinum-iridium inoculating needles and stabbing them into deep slants containing a reduced amount of agar. The main concentration of cells in the water of syneresis and in the top part of the agar at the base of the slant allowed even small colonies of the more

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Biographical Memoirs: Volume 81 fastidious anaerobes to grow. It also provided an excellent menstrum for preparing wet mounts for study of cell morphology and motility with the phase-contrast microscope. Marv used various modifications for studying anaerobic bacteria as diverse as methanogens, photosynthetic bacteria, sulfate reducers, human GI tract anaerobes, and those of medical concern. A large number of bacterial strains were first isolated and enumerated from dairy cattle fed diverse diets, such as hay, hay-concentrate, and forage-crop silage. These strains were studied for morphology and a few physiological features and were placed in tentative groups. Selected strains were then placed in a dry-ice cabinet so that live cultures could be maintained for detailed biochemical and nutritional studies. Unlike Hungate, Marv firmly believed that one of his most important functions was maintaining the culture collection of rumen anaerobes, many of which were later well documented as important in anaerobic degradation, and making them available to other researchers around the world. With the continuity of support at Beltsville and later at the University of Illinois he was able to continue this function. For about 20 years his group was the main and often the only source of many rumen anaerobes. Among the important bacteria described in detail were many cellulolytic strains of B. succinogenes, which until detailed studies were done seemed morphologically quite different from Hungate’s strains. Marv later showed that this species degraded highly resistant crystalline cellulose much faster than other known mesophilic anaerobic cellulolytic bacteria. Large numbers of cellulolytic strains of Ruminococcus albus and R. flavefaciens were studied and the work also emphasized the importance of these in xylan fermentation and the importance of ethanol formation in R. albus versus succinate formation in R. flavefaciens. The

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Biographical Memoirs: Volume 81 genus Butyrivibrio was named and great versatility in production of CO2, lactate, and butyrate and in fermentation of important carbohydrates was found, as well as considerable variation between strains. Only a few strains fermented cellulose, but most fermented xylan, starch, pectin, and many other carbohydrates. Later work at Illinois in association with Jones, Cheng, and Simpson from Canada showed that some strains fermented important plant flavonoids. This work represented the first pure culture demonstration of anaerobic degradation of the aromatic heterocyclic ring structure. Bacteroides ruminicola, one of the most numerous and versatile of rumen bacteria, was isolated and described. This succinate and acetate-producing species fermented complex carbohydrates including various pentosans, pectin, and starch, as well as many sugars. It was actively proteolytic and could convert amino acids, derived from peptides transported into the cell, into ammonia, CO2, and various straight- and branched-chain volatile fatty acids. Selenomonas ruminantium had been observed microscopically in rumen contents as early as 1889 because of its unique morphology and relatively large size and was obtained in pure culture but not recognized by Huhtanen and Gall in 1953. Marv isolated and identified this important rumen species, which produced various amounts of propionate, acetate, lactate, and CO2 from many different sugars and starch and also degraded a number of amino acids. The subspecies lactilytica fermented important energy sources such as lactic acid and glycerol. S. ruminantium became one of the organisms most used by workers at Illinois and elsewhere in rumen microbiological studies. For example, Marv used it to examine various interactions between species, the effect of factors such as growth rate on the types of fermentation products, the various enzyme sys-

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Biographical Memoirs: Volume 81 tems involved in ammonia assimilation, and regulation of urease production. A number of additional new species and often new genera involved in various rumen reactions were also described. These included the butyrate-forming Eubacterium cellulosolvens, pectin-fermenting Lachnospira multiparus, xylan-fermenting Eubacterium ruminantium, and the succinate- and acetate-forming Succinivibrio dextrinosolvens and Succinimonas amylolytica. Rumen flora developing in young calves were studied concurrently with the detailed investigations of bacteria from mature animals. The studies of the flora of young calves gave Marv further insight into the diversity of anaerobic bacteria and the difficulty of identifying well-studied strains from previously published descriptions, which were still very poor in 1958. Most of the large number of anaerobes in calves one to three weeks old differed substantially from those in mature animals and Marv decided not to name them. However, it became possible to identify most representative strains, partly because of the efforts of W. E. C. Moore and his colleagues at the Anaerobe Laboratory of Virginia Polytechnic Institute. One of the most important strains that Marv identified in young calves was Fusobacterium necrophorum. Although long known as a pathogen and major cause of liver abscesses in cattle, it was not known as a major normal organism fermenting lactate, amino acids, and sugars and producing butyrate and other acids in young calves. Another important strain was Clostridium clostridiiforme, an organism whose spores were very hard to detect. It had been found in several pathologic processes and as a normal poultry intestinal isolate but had not been previously found in the rumen. Marv’s group, as well as workers in Scotland, discovered the long form of Lactobacillus vitulinus in young calves. This organism obviously differed from the short form found

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Biographical Memoirs: Volume 81 in older calves and adult ruminants. Both Marv and the Scottish workers also described the lactate-fermenting, amino-acid-catabolizing Megasphaera elsdenii that had been studied in detail by Elsden and Lewis in 1953. In addition, the lactate-fermenting Eubacterium limosum (Butyribacterium rettgeri) was detected in the rumen for the first time. This organism was of interest because of its ability to produce butyrate and longer-chain volatile fatty acids from one-carbon compounds such as methanol or H2-CO2. The studies of pure cultures of functional rumen bacteria disclosed large numbers of species that produced such products as lactate and ethanol, which were not normal products or important extracellular intermediates in the rumen fermentation. Some microbiologists believed, because these “artifacts” occurred, that the pure cultures were not worth studying. However, Marv’s view was that judicious studies of pure cultures and known mixtures were valuable because they would yield important facts about the environmental factors causing the abnormalities that would be impossible to find with studies on the total fermentation. These facts in turn would lead toward better knowledge about regulation of the rumen fermentation. Later work at Illinois and elsewhere strongly supported Marv’s view. After initiating the studies on numbers and kinds of rumen bacteria, Marv was joined by Nola Small, an outstanding technical assistant. As a result, he had time to do detailed studies on the nutrition of pure cultures. Hungate’s studies had shown that a number of rumen cellulolytic species required unknown growth factors that were present in rumen fluid but not in rich sources of vitamins and other growth factors such as liver or yeast extract. Marv found that the factor required by B. succinogenes had two components. A straight-chain saturated fatty acid, n-valerate, or longer-chain acids satisfied one component, and a branched-

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Biographical Memoirs: Volume 81 student Mike McInerney, co-cultures of Methanosarcina (an organism that produces methane from both H2-CO2 and acetate) and Desulfovibrio completely dissimilated lactate or ethanol to methane and CO2. More important, the degradation of acetate by the Methanosarcina was repressed until after the organism had utilized the H2 that the Desulfovibrio produced while dissimilating the primary substrate to acetate. This finding was relevant to understanding the fact that although Methanosarcina is present in the rumen, it uses H2-CO2 (and probably methanol and methylamines) as energy source in preference to acetate degradation except under adverse conditions of very long rumen retention times and extremely low H2 levels. Marv had worked for many years without success to prove via isolation of co-cultures that propionate and longer-chain fatty acids were anaerobically degraded in nature by syntrophic associations of fatty acid oxidizers with H2 utilizers. Success was finally achieved in 1976, while he was on sabbatical leave with Norbert Pfennig in Germany. The success was due to the use of the fatty acid oxidizers with sulfate-reducing Desulfovibrio as the H2 user in place of M. ruminantium, the former apparently having much greater affinity for H2 than the latter at the slow growth rate necessary for the fatty acid degrader. After the initial success the project was expedited by McInerny. The organism, which was named Syntrophomonas wolfei, beta-oxidizes fatty acids producing H2 and either acetate (from fatty acids with even-numbered carbon atoms) or acetate and propionate (fatty acids with odd-numbered carbon atoms) in obligate syntrophy with H2-using methanogens such as M. hungatei, Methanosarcina, or H2-using Desulfovibrio. This was the first description of pure co-cultures of anaerobic bacteria that degrade fatty acids. Later, postdoctoral associate David Boone isolated a propionate-decarboxylating, acetate-producing

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Biographical Memoirs: Volume 81 species that he and Marv called Syntrophobacter wolinii. This organism required syntrophic conditions similar to those of S. wolfei. Marv’s graduate student Vincent Varel found that thermophilic methane production could be started up from bacteria in cattle waste in a period of about 12 days, a much shorter time than previously thought possible. They obtained a faster methanogenesis with higher loading of cattle waste into digestors than any previous group had achieved. The work was continued by research associate Rod Mackie who greatly expanded the knowledge of the kinetics of fatty acid degradation, bacterial growth, and protein synthesis in cattle-waste methanogenesis at both mesophilic and thermophilic temperatures. Although ruminant nutritionists had long been interested in the amount of microbial cells and protein synthesized in the rumen in relationship to the amount of organic matter the microbes digested, considerable difficulty was involved in accurately determining this in vivo, and yield values from various laboratories gave variable results. In cooperation between Marv’s laboratory and those of Frank Hinds and Fred Owens (Department of Animal Science), Ronald Isaacson set up model experiments with continuous cultures of mixed rumen bacteria growing on glucose to determine the efficiency of rumen bacterial growth in relationship to the rate of passage of material through the system. They found that at dilution rates covering the range expected in the rumen, the bacterial protein yield varied as much as two-fold. This variation emphasized the importance of the bacterial maintenance energy requirement in net growth of rumen bacteria. As rates of passage increased, more of the energy of the digested material available to the ruminant animal was used for growth and synthesis of microbial protein. This concept was later exploited in many

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Biographical Memoirs: Volume 81 laboratories to improve the efficiency of protein synthesis by rumen microbes. Identity of the bacteria active in urea hydrolysis to ammonia and CO2 via the production of urease in the rumen was long unknown. In the early 1980s Marv assigned Isaacson the special problem of selectively isolating major ureaseforming bacteria, by use of urea as the main possible N source in a chemically defined medium. They theorized that the bacteria might not form urease in the presence of much ammonia or other rapidly used N source present in the growth medium. They successfully isolated a urease-producing bacterium that was shown by graduate student Andrew John to be a somewhat atypical variety of Selenomonas ruminantium. In this strain, urease was indeed strongly repressed by large amounts of urea, ammonia, or amino acids. Varel, using similar isolation techniques, showed that the human bowel organism, Peptostreptococcus productus, present in huge numbers in human feces, had similar urease activity. Graduate student Mary Ann Wozny then developed a rapid assay and growth medium in which most pure cultures of fermentative anaerobes grew and expressed urease activity. In screening many nonselectively isolated strains from the rumen and human species, she confirmed Varel’s results with feces and found more human fecal anaerobes forming urease as well as more rumen species. Such strains were found to be predominantly from cattle maintained on high grain diets with unusually low levels of crude protein and thus low rumen ammonia levels. The strains were sent by Marv to Virginia Polytechnic Institute and identified as S. dextrinosolvens, Treponema spp and Ruminococcus bromii. Further studies with graduate student C. J. Smith and colleague R. B. Hespell, Marv studied urease regulation and enzymology of ammonia assimilation in S. ruminantium. The first enzyme of ammonia

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Biographical Memoirs: Volume 81 assimilation was found to be glutamate dehydrogenase, which required little energy for ammonia assimilation but which had poor affinity for ammonia and was much less active at low ammonia levels. An alternative route was the glutamine synthetase-glutamate synthase system, which had a very high affinity for ammonia but required some of the energy otherwise available for the growth of the bacterium. Both the urease and the glutamine synthetase were strongly repressed when the growth rate was limited by the amount of energy source in the medium rather than by the ammonia level. Marv and coworkers hypothesized that synthesis of both urease and glutamine synthetase was regulated by a common gene product. There was considerable controversy concerning the concentration of ammonia necessary in the rumen to ensure maximum growth rate and yield of the fermentative rumen bacteria. Marv, along with graduate student Dan Schaefer and Professor Carl Davis, proved that important rumen bacterial species had a great affinity for ammonia as nitrogen source and could achieve maximum growth rates with 1 mM or less ammonia. Marv’s graduate student Bill Brulla, in association with Professor Smith, studied the improved feed efficiency in cattle fed the bacterial antibiotic monensin. Furthermore, the nutrition of gastrointestinal tract anaerobes remained of interest to Marv. Janice Herbeck and he showed that the nutrient requirements of R. bromii, one of the main species digesting starch in humans and in ruminants fed large amounts of grain, were very similar to those of the cellulolytic R. albus. Varel determined the simple nutritional requirements of Bacteroides fragilis, the most numerous species in humans, a major starch and hemicellulose fermenter, and an opportunistic pathogen in compromised humans. The minimal medium developed by Varel and Marv

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Biographical Memoirs: Volume 81 has since been used in many ecological, genetic, and pathology research laboratories. Marv had long suspected that some important rumen bacteria had a growth requirement for a fat-soluble vitamin of the vitamin K group. Undergraduate student Colleen O’Dowd and graduate student Jane Leedle established this for Succinivibrio and Rogelio Gomez-Alarcon of Marv’s group found 1,4-naphthaquinone to be the most active. Marv’s undergraduate student H. G. Betian and graduate student Barbara Lineham found large numbers of cellulolytic bacteria in the bowel microbiota in some young adult humans and isolated a new species of Bacteroides. Their finding of populations as high as 108 cellulolytic bacteria per g of feces had never been observed before in the bowel. In another collaboration with Professor Davis, Barbara Genthner found that a lactate fermenter, Eubacterium limosum, which had been found earlier by Marv to exist only in the rumen of very young calves, was a very dominant organism in the rumen of sheep fed sugar cane molasses as their main energy source; it was also found to be a significant component in anaerobic digestors of domestic sewage. They established that the organism produced acetate and butyrate and some fatty acids with longer chains when it fermented the one-carbon compound methanol (from pectin breakdown) and H2-CO2. It also fermented branched-chain amino acids to branched-chain fatty acids, which were shown to be the major microbial products in the rumen of molasses-fed animals. Marv served his scientific community well. He was the editor in chief of the Journal of Applied and Environmental Microbiology from 1967 to 1980 and was a member of the Board of Trustees of Bergey’s Manual of Determinative Bacteriology from 1975 to 1986. He was a member of the American Society for Microbiology and the American Dairy

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Biographical Memoirs: Volume 81 Science Association and a fellow of the American Association for the Advancement of Science and the American Academy of Microbiology. He also was a member of Phi Beta Kappa, Phi Kappa Phi, and Sigma Xi honor societies. For his contributions to science he received the Superior Service Award of the U.S. Department of Agriculture in 1959; the Borden Award of the American Dairy Science Association in 1978; the Paul A. Funk Award of the University of Illinois in 1979; the Fisher Award of the American Society for Microbiology in 1986; election to the National Academy of Sciences in 1987; the Alumni Achievement Award of Washington State University in 1991; and the Bergey’s Medal for Distinguished Achievement in Bacterial Taxonomy in 1996. He also was made honorary member of the American Society for Microbiology, the highest honor awarded by that society. In reviewing his many years of work in rumen and related anaerobic bacteriologic research, Marv concluded as follows: I became increasingly aware of my good fortune in having selected an area of work in which I have some innate competence and in having been at the right places at the right times to be associated with many outstanding, creative, unselfish colleagues whose main goals in life have been to advance the science of anaerobic bacteria and related areas in a holistic, unparochial, objective manner. I have also been very fortunate to have worked with administrators who put up with my somewhat juvenile personality and left me in the position that the major deterrents to achievement have been my own inadequacies. My wife, Margaret, has been the strong pillar of love and support essential to my progress. Marv was the gentle giant of rumen microbiology. There was a special light in his eyes and a special tone to his voice when his beloved rumen bacteria were being discussed. He was a national treasure of information on anaerobes and

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Biographical Memoirs: Volume 81 his colleagues at Illinois and all over the world benefited from his presence. Marv is survived by his wife, Margaret, of 54 years; sons Robert M. Bryant of Livermore, California, and Steven E. Bryant of Champaign, Illinois; daughters Margaret (“Peggy”) Bryant of Pleasanton, California, Susan J. Bryant of Olympia, Washington, and Katherine B. Smith of Maple Plain, Minnesota; sister June Chambers of Boise, Idaho; and nine grandchildren. MOST OF THE information in this article was derived from an autobiographical article written in 1980 by Marvin P. Bryant in honor of his receipt of the Paul A. Funk Award of the University of Illinois. He titled it “Marvin P. Bryant, A Rumen Microbiologist.”

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Biographical Memoirs: Volume 81 SELECTED BIBLIOGRAPHY 1956 The characteristics of strains of Selenomonas isolated from bovine rumen contents. J. Bacteriol. 72:162-67. 1958 With M. J. Allison and R. N. Doetsch. Volatile fatty acid growth factor for cellulolytic cocci of the bovine rumen. Science 128:474-75. 1959 Bacterial species of the rumen. Bacteriol. Rev. 23:125-53. With I. M. Robinson and H. Chu. Observations on the nutrition of Bacteriodes succinogenes—a ruminal cellulolytic bacterium. J. Dairy Sci. 42:1831-37. 1961 With I. M. Robinson. Some nutritional requirements of the genus Ruminococcus. Appl. Microbiol. 9:91-95. 1962 With I. M. Robinson. Some nutritional characteristics of predominant culturable ruminal bacteria. J. Bacteriol. 84:605-14. 1963 With I. M. Robinson. Apparent incorporation of ammonia and amino acid carbon during growth of selected species of rumen bacteria. J. Dairy Sci. 46:150-54. 1964 With R. E. Hungate and R. A. Mah. The rumen bacteria and protozoa. Annu. Rev. Microbiol. 18:131-66. 1967 With E. A. Wolin, M. J. Wolin, and R. S. Wolfe. Methanobacillus omelianskii: A symbiotic association of two species of bacteria. Archiv. Mikrobiol. 59:20-31

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Biographical Memoirs: Volume 81 1972 With C. A. Reddy and M. J. Wolin. Characteristics of S organism isolated from Methanobacillus omelianskii. J. Bacteriol. 109:539-45. 1973 Nutritional requirements of the predominant rumen cellulolytic bacteria. Fed. Proc. 32:1809-13. 1975 With S.-F. Tzeng and R. S. Wolfe. Factor 420-dependent pyridine nucleotide-linked hydrogenase system of Methanobacterium ruminantium. J. Bacteriol. 121:184-91. 1977 Microbiology of the rumen. In Dukes’ Physiology of Domestic Animals, 9th ed., ed. M. P. Swenson, pp. 187-304. Ithaca, N.Y.: Cornell University Press. With L. L. Campbell, C. A. Reddy, and M. R. Crabill. Growth of Desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl. Environ. Microbiol. 33:1105-12. With C. A. Reddy. Deoxyribonucleic acid base composition and cytochromes of certain species of the genus Bacteroides. Canad. J. Microbiol. 23:1252-56. 1979 Microbial methane production—theoretical aspects. J. Anim. Sci. 48:193-201. With R. B. Hespell. Efficiency of rumen microbial growth: Influence of some theoretical and experimental factors on YATP. J. Anim. Sci. 49:1640-59. 1980 With D. R. Boone. Propionate-degrading bacterium, Syntrophobacter wolinii sp. nov., gen. nov. methanogenic ecosystems. Appl. Environ. Microbiol. 40:626-32.

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Biographical Memoirs: Volume 81 1981 With M. J. McInerney. Anaerobic degradation of lactate by syntrophic associations of Methanosarcina barkeri and Desulfovibrio and effect of H2 on acetate degradation. Appl. Environ. Microbiol. 41:346-54. 1986 The genus Ruminococcus. In Bergey’s Manual of Systematic Bacteriology, vol. 2, ed. P. Sneath, pp. 1093-97. Baltimore: Williams and Wilkins. With T. L. Miller, M. J. Wolin, and H. Zhao. Characteristics of methanogens isolated from bovine rumen. Appl. Environ. Microbiol. 51:201-202. 1987 With D. R. Boone. Isolation and characterization of Methanobacterium formicicum MR. Int. J. Syst. Bacteriol. 37:171. 1990 With R. I. Mackie. Efficiency of bacterial protein synthesis during anaerobic degradation of cattle waste. Appl. Environ. Microbiol. 56:87-92. 1993 With H. Zhao, D. Yang, and C. R. Woese. Assignment of fatty acid-β-oxidizing syntrophic bacteria to Syntrophomonodaceae fam. nov. on the basis of 16S rRNA sequence analyses. Int. J. Syst. Bacteriol. 43:278-86. 1994 With R. I. Mackie. Acetogenesis and the rumen: Syntrophic relationships. In Acetogenesis, ed. H. L. Drake, pp. 331-364. New York: Chapman-Hall.

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Biographical Memoirs: Volume 81