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Biographical Memoirs: Volume 61 This page in the original is blank.
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Biographical Memoirs: Volume 61 PERRY WILLIAM WILSON November 25, 1902-August 17, 1981 BY ROBERT H. BURRIS PERY WILSON, more than any other individual, turned studies of biological nitrogen fixation from a descriptive to a quantitative and analytical emphasis. Nitrogen deficiency more frequently limits plant growth than does any other deficit except water. Certain procaryotic organisms can convert nitrogen from the atmosphere to a form that plants can use. Wilson's research laid the groundwork for the phenomenal increase in studies on the biochemistry, genetics, and physiology of biological nitrogen fixation, a process vital to maintenance of the nitrogen cycle on earth. Perry William Wilson was born in Bonanza, Arkansas. The family moved from Bonanza to Oklahoma and thence to Terre Haute, Indiana, when Perry still was very young. The possessions and income of the family were modest. Perry Wilson, in an autobiographical sketch introducing the 1972 Annual Reviews of Microbiology about ''Training a Microbiologist,'' said, My thesis is that one's training comes from many sources, none of which should be overlooked or overemphasized. A widely held belief is that one's career often reflects early influences. As the twig is inclined. My own early training can hardly furnish a test case since I never attended a school long enough to become inclined toward anything. A member of a
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Biographical Memoirs: Volume 61 somewhat mobile family, I attended elementary schools in Arkansas, Oklahoma and Indiana, none for a period of more than two years. The curriculum in such schools was based largely on the three Rs—I became proficient in only two—reading and arithmetic. Biology consisted of courses in human physiology decorously taught from a text suitable for a mixed audience. The text and illustrations were studiously neutral with respect to reproduction. However, such deficiencies mattered not at all; to a student body made up largely of farm children, the facts of life were a part of their daily experience. My favorite course was arithmetic. The problems were oriented toward the practical. In a culture where a mortgage on crops and land was another fact of life, a great deal of attention was given to the calculation of partial payments on bank loans ... High school was different. Our family finally settled in Terre Haute, Indiana, and I had the unique experience of attending all four years in an excellent high school. It was staffed by a group of well-trained, young, enthusiastic teachers; they inspired many of us to dream of such a career. In my senior year I took chemistry, but the experience did not alter my plans for a career: attend the local teacher's college and become a professor of high school mathematics. After completing his high school work in 1920, Perry Wilson received a college scholarship, but it was inadequate to cover expenses, so he took a job as lab boy at the Commercial Solvents Corporation (CSC) in Terre Haute. There had been a great demand during World War I for acetone for use in explosives and in "dope" for airplane wings, and Commercial Solvents had erected a butanol-acetone fermentation plant in Terre Haute. They used Chaim Weizmann's culture of Clostridium acetobutylicum which produced butanol, acetone and ethanol in the proportions 60:30:10. Although the demand for acetone slackened after the war, the demand for butanol expanded as a market was created for it in automobile lacquers, so the plant continued to operate. Perry's first job at CSC was to collect samples periodically from the various tanks being used for production of inoculum for the 40,000-gallon fermentation tanks of corn mash. The distillation of solvents was done from copper
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Biographical Memoirs: Volume 61 pots, and Perry enjoyed keeping them bright. Mr. Bogin, the supervisor, took an interest in Perry, loaned him books, and taught him analytical methods. After a period in the fermentation lab, Perry's career goals shifted away from teaching high school mathematics, so in the fall of 1922 he enrolled as a chemical engineering student at Rose Polytechnic Institute in Terre Haute. He continued to work weekends at CSC. The butanol fermentations often would become sluggish, and the yield of solvents would drop precipitously; the basis of the difficulty was baffling. Because of their backgrounds in microbiology and fermentation, E. B. Fred and I. L. Baldwin, members of the bacteriology staff at the University of Wisconsin, were invited by CSC to serve as consultants. They uncovered the fact that some of the difficulties with the fermentations arose from contamination with Lactobacillus leichmannii. The plant was a remodeled distillery and had a maze of pipes, valves, and dead ends that never were adequately heated by the steam used for sterilization. When the cul-de-sacs were eliminated in a new plant designed by industrial engineers, this problem with contamination was eliminated. However, some fermentations still became sluggish, and it was only later that the source of the problem was defined. Wilson was offered a position as analytical chemist at the CSC plant, so he dropped out of school for a year to take the job. This gave him a chance to become acquainted with consultants to the company, as he was responsible for analyses of the experimental fermentations. The company sold fermentation residues as an animal feed, and Perry did the nitrogen analyses to establish that the protein content of the material met standards. Perry studied for another year at Rose Polytechnic Institute and then returned to CSC in the lacquer research
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Biographical Memoirs: Volume 61 department. There he became involved further in analytical organic chemistry. In the fall of 1925 he was told that the company was going to establish some research fellowships at the University of Wisconsin under the direction of Professors Fred and Peterson. This interested him immediately because he had been indoctrinated on Wisconsin by three Wisconsinites on the research staff, and he was well acquainted with Fred and Peterson from their consulting work at the Terre Haute plant. As Perry still was an undergrad, Fred and Peterson did the necessary bending of the fellowship rules so he could complete his undergraduate work at the University of Wisconsin. So he transferred for the second semester in 1926 and was granted fifty credits for his work at Rose Polytechnic Institute. His record shows that he later was permitted to substitute organic chemistry for physiology, physical chemistry for animal husbandry, and math for an agriculture option. His agriculture course record shows that he took bacteriology, agricultural chemistry, agronomy, botany, chemistry, economics, English, German, and veterinary science. It is evident that he designed a program to give himself a solid background in basic sciences. Although Perry's previous training had included little biology, the course in bacteriology by W. H. Wright captured his imagination, and he wondered how effectively he could integrate his bent for chemistry with a career in bacteriology. The broad treatment of bacteriology in E. B. Fred's soil bacteriology course convinced him that microbiology was broad enough to cover a whole spectrum of interests. His minor was biochemistry (agricultural chemistry at that time), and he took courses from Hart, Steenbock, Peterson, and Tottingham. For research, Wilson was assigned the task of identifying crystals recovered by Elizabeth McCoy from milk that had been fermented by butyric
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Biographical Memoirs: Volume 61 acid organisms. The crystals were calcium citrate, but when they determined the water of crystallization, they found that the literature value was incorrect. So in 1927 Peterson, Wilson, McCoy, and Fred published a paper, Perry's first, in the Journal of the American Chemical Society to correct the value. In the summer, Perry returned to CSC and was assigned to the bacteriological research division. There he worked with D. A. Legg, who had diagnosed that the sluggish fermentations had been caused by a bacteriophage, then described as the d'Herelle phenomenon. A phage-resistant strain solved the difficulties. Perry received his B.S. in 1928 and submitted an undergraduate thesis project, "Production of Acetylmethyl Carbinol by Clostridium acetobutylicum." In September 1928, Perry Wilson returned to Madison to initiate his graduate studies. He continued work in bacteriology and agricultural chemistry under the direction of E. B. Fred and W. H. Peterson, and investigated the nitrogen metabolism of Clostridium acetobutylicum, the CSC organism. He intended to return to CSC the next year, but his career was altered at this point. In the spring of 1929, the Frasch Foundation, through the American Chemical Society, awarded $40,000 to the departments of Agricultural Chemistry and Bacteriology to do research over a period of five years on the biochemistry of microorganisms. Half the award was for investigating the biochemistry of symbiotic nitrogen fixation. Professors Fred and Peterson asked Perry, when he had finished his M.S. work in the summer, to shift to the Frasch grant and start working on biological nitrogen fixation. This would delay Perry's Ph.D. for a year but would carry an increased stipend. He reasoned that he could finish his Ph.D. and then go back to industrial fermentation, so he accepted. He neglected to
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Biographical Memoirs: Volume 61 take into account how an intriguing research problem and its many ramifications can keep one bound and occupied for life—he never returned to industrial fermentation. Perry Wilson completed his M.S. degree in August 1929. He married Helen Evelyn Hansel on September 4, and they settled in Madison so Perry could complete his Ph.D. Theirs was a happy marriage. Perry was inherently a nervous and constantly active person, and it was up to Helen to try to keep things on an even keel. As Helen opined later, "Life with Perry was always exciting, sometimes a little hectic, but never dull." Back in the laboratory in the fall of 1929, Perry started to learn about growing plants, as his research was to focus on fixation in leguminous plants. To keep occupied during this learning period, he wrote a theoretical paper on the energetics of heterotrophic bacteria with W. H. Peterson and published it in Chemical Reviews—his first review. Perry had taken an undergrad course with Warren Weaver on probability and had found it a thoroughly exciting experience. He also had taken a stimulating course on the mathematical foundations of statistics from Mark Ingraham, and this had prompted him to read the work of R. A. Fisher and others. He teamed up with Ethel Kullman, who was examining methods for counting the rhizobia, and they published a statistical inquiry into methods for estimating rhizobia. With the plant methods under reasonable control, Perry Wilson launched into his Ph.D. studies on the relationship between the concentration of carbon dioxide and the fixation of nitrogen by alfalfa and clover. He completed his Ph.D. in 1932 and submitted a thesis on the biochemistry of nitrogen fixation by the legumes. It is apparent that he had lived up to the expectations of E. B. Fred, W. H. Peterson, and I. L. Baldwin, and after his Ph.D. was awarded, the
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Biographical Memoirs: Volume 61 Bacteriology Department appointed him as an instructor in 1932, followed by advancement to assistant professor in 1934, associate professor in 1938, and professor in 1943. The Chemistry Department had wanted a course to acquaint their students with biological science. Bacteriology was willing to accommodate, and Perry was assigned to develop a lecture and lab course that was designed primarily for senior chemistry majors. This course, which appeared under various numbers during forty years, was "Perry's baby." It was more demanding than the usual general course in bacteriology and attracted students who wanted a challenge. After some years, it was taken by most seniors in pharmacy as well as chemistry, and it drew many other students with good science backgrounds. It is interesting that Ed Tatum, future Nobel Laureate, early volunteered to aid in the lab to gain teaching experience. From time to time Perry also taught soil microbiology, bacterial physiology, history of bacteriology, and a course in writing scientific reports. To back up a bit, biological nitrogen fixation had received considerable attention, because the importance of nitrogen as a major fertilizer element for plants had been recognized widely. Mixing a leguminous crop with a non-leguminous crop was practiced as a beneficial operation in the time of the Romans, but the basis of the benefit was not clear. Boussingault in the 1830s performed careful field experiments that convinced him that leguminous plants, such as peas, accumulated considerably more nitrogen than non-leguminous controls, and he suggested that the nitrogen was derived from air. Liebig, who was the leading organic chemist of the day, assailed the findings of Boussingault without bothering to do any experiments to check their validity. This voice of authority from Germany convinced many, but not all; the French continued to support Boussingault. Lawes, Gilbert, and Pugh in England attempted
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Biographical Memoirs: Volume 61 to resolve the issue with very carefully performed experiments, but their careful preparations destroyed the nitrogen-fixing bacteria upon which the legumes depend. Finally, in 1886, Hellriegel and Wilfarth in Germany reported convincing evidence that nodulated leguminous plants can utilize molecular nitrogen. The information was rather quickly reduced to agronomic practice, and in time it became an accepted practice to inoculate leguminous seeds with suitable root nodule bacteria at the time of planting, so that their roots would become properly infected to form nodules. The period 1886 to 1932 was marked by the isolation of root nodule bacteria (Rhizobium sp.) in pure culture, demonstration of their specificity for certain leguminous plants, study of the physiology of the organisms, investigation of the infection process, and attempts to get the rhizobia to fix nitrogen apart from the host plant. The biochemistry of nitrogen fixation was largely neglected. Dean Burk had the idea that this would be a fascinating area of study, so as a postdoc in Meyerhofs lab, he launched studies on the free-living, aerobic nitrogen fixer Azotobacter chroococcum. He utilized manometric techniques to investigate the respiration of the organism and attempted to establish its response to changes in the pO2 and pN2. Burk stayed with these studies for about a decade and then shifted his research to an even more elusive subject, cancer. Although the constants reported by Burk were not very accurate, he established a new approach for studies of nitrogen fixation. The unity of biochemistry was being stressed, and Perry was intrigued by the possibilities in developing the comparative biochemistry of nitrogen fixation. He chose the leguminous plant system rather than a free-living nitrogen fixer for investigation. Perhaps this was because the Frasch grant specified work with legumes. The complex symbi-
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Biographical Memoirs: Volume 61 otic system is much more difficult to manipulate experimentally than an organisms such as A. chroococcum, but as Perry stated on the occasion of receiving the Pasteur Award in his lecture "Chance Favors the Prepared Mind," The first piece of luck arose because we chose the wrong experimental material with which to make the study—the symbiotic system of leguminous plants and the root nodule bacteria. Today we realize that this system is far too complicated for an initial survey and that we should have used species of the free-living soil bacteria, either Azotobacter or Clostridium. But had we done so, we undoubtedly would have missed the significant observation that gave us the break we needed. The break to which he referred was the discovery that hydrogen is a specific and competitive inhibitor of nitrogen fixation. Red clover inoculated with Rhizobium trifolii was chosen as the experimental plant. The seeds were surface sterilized, and after being germinated aseptically they were inoculated and transferred to 9-liter Pyrex serum bottles containing sand with plant nutrient minus nitrogen. The cotton stoppers that had been in place for sterilization of the units were replaced with stopper assemblies that allowed evacuation and gas addition through cotton filters. Units were evacuated, and gases were added to desired pressures. An internal indicator showed when it was necessary to add carbon dioxide. Other gases were changed weekly, and plants were grown about six weeks before harvesting. Although the technique of growing plants in closed containers under controlled gas atmospheres was time-consuming, it yielded interesting results, most of which were summarized by P. W. Wilson in his 1940 monograph "The Biochemistry of Symbiotic Nitrogen Fixation." In approximately a decade, Perry and his research group had defined
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Biographical Memoirs: Volume 61 the growth substance requirements of the rhizobia, studied the respiration of the organisms, investigated and disproved claims that aseptic germinating legume seeds fix nitrogen, investigated the carbohydrate-nitrogen relationship, established the effects of carbon dioxide and light intensity on fixation, checked the claims for excretion of nitrogen from legume roots, established the pN2 function and the pO2 function in nitrogen fixation, determined the Michaelis constant for nitrogen fixation in red clover, studied the associated growth of legumes and non-legumes, and reported on the energetics of nitrogen fixation. Perry's monograph summarized this research, and its publication became a milestone in biological nitrogen fixation and a worthy successor to the 1932 monograph of Fred, Baldwin, and McCoy entitled "The Root Nodule Bacteria and Leguminous Plants." The decade of the thirties included a year when Perry Wilson did research abroad on a Guggenheim fellowship. In his letter supporting Perry's application for the Guggenheim fellowship, E. B. Fred stated, "Perry Wilson possesses an unusual capacity for productive scholarship. He is a clean-cut young man of sterling qualities. In my opinion he is the most promising young man in the field of the biochemistry of microorganisms which we have ever had at Wisconsin." In 1936, the Wilsons went to Cambridge, England, on the Guggenheim fellowship. There Perry worked with Marjory Stephenson's group to test whether hydrogenase was somehow associated with biological nitrogen fixation. His stay there also provided an opportunity to learn about enzymology and enzymological methods. Perry utilized manometric techniques in his studies, and upon his return to Madison acquired a Warburg respirometer unit for his lab. Cambridge was a hotbed of activity in enzymology, both in
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Biographical Memoirs: Volume 61 With E. B. Fred and M. R. Salmon. Relation between carbon dioxide and elemental nitrogen assimilation in leguminous plants. Soil Sci. 35:145-65. With P. Wenck and W. H. Peterson. A statistical study of nitrogen fixation by clover plants. Soil Sci. 35:123-43. 1934 With E. B. Fred. On photosynthesis and free nitrogen assimilation by leguminous plants Proc. Natl. Acad. Sci. USA 20:403-9. 1935 With F. S. Orcutt. The effect of nitrate-nitrogen on the carbohydrate metabolism of inoculated soybeans. Soil Sci. 39:289-96. With E. M. Smyth. Uber die scheinbare Stickstoffassimilation keimender Erbsen. Biochem. Z. 282:1-25. The carbohydrate-nitrogen relation in symbiotic nitrogen fixation Wis. Agric. Exp. Stn. Res. Bull. 129:40 pp. With E. B. Fred. The growth curve of a scientific literature—Nitrogen fixation by plants. Sci. Mon. 41:240-50. 1936 With F. S. Orcutt. Biochemical methods for the study of nitrogen metabolism in plants Plant Physiol. 11:713-29. With W. W. Umbreit. Determination of basic nitrogen. Ind. Eng. Chem. Anal. Ed. 8:361-62. Mechanism of symbiotic nitrogen fixation. I. The influence of pN2. J. Am. Chem. Soc. 58:1256-61. Uber die scheinbare Stickstoffassimilation keimender Erbsen. Biochem. Z. 287:418-19. 1937 Excretion of nitrogen by leguminous plants. Nature 140:154. Symbiotic nitrogen-fixation by the leguminosae. Bot. Rev. 3:365-99. With J. C. Burton and V. S. Bond. Effect of species of host plant on nitrogen fixation in Melilotus J. Agric. Res. 55:619-29. With E. B. Fred. Mechanism of symbiotic nitrogen fixation. II. The pO2 function. Proc. Natl. Acad. Sci. USA 23:503-8. With W. W. Umbreit. Mechanism of symbiotic nitrogen fixation. III. Hydrogen as a specific inhibitor. Arch. Mikrobiol. 8:440-57. With W. W. Umbreit. Fixation and transfer of nitrogen in the soy-
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Biographical Memoirs: Volume 61 bean Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 2 96: 402-11. With F. C. Wagner. Combined nitrogen and the nitrogen fixation process in leguminous plants. Trans. Wis. Acad. Sci. Arts Lett. 30: 43-50. With O. Wyss. Mixed cropping and the excretion of nitrogen by leguminous plants Soil Sci. Soc. Proc. 2:289-97. 1938 With P. M. West. Synthesis of growth factors by Rhizobium trifolii. Nature 142:397. With P. M. West. Biological determination of vitamin B1 (thiamin) in Rhizobium trifolii. Science 88:334-35. Respiratory enzyme systems in symbiotic nitrogen fixation. I. The "resting cell" technique as a method for study of bacterial metabolism J. Bacteriol. 35:601-23. With J. C. Burton. Excretion of nitrogen by leguminous plants. J. Agric. Sci. 28:307-23. With W. W. Umbreit and S. B. Lee. Mechanism of symbiotic nitrogen fixation. IV. Specific inhibition by hydrogen. Biochem. J. 32: 2084-95. 1939 With R. H. Burris. Respiratory enzyme systems in symbiotic nitrogen fixation. Cold Spring Harbor Symp. Quant. Biol. 7:349-61. With J. C. Burton. Host plant specificity among the Medicago in association with root nodule bacteria. Soil Sci. 47:293-303. With C. A. Elvehjem, ed. Respiratory Enzymes. Minneapolis: Burgess, 236 pp. With W. W. Umbreit. Studies on the mechanism of symbiotic nitrogen fixation. Trans. Third Comm. Int. Soc. Soil Sci., vol. A, pp. 29-31. With P. M. West. The relation of "Coenzyme R" to biotin. Science 89:607-8. With P. M. West. Growth factor requirements of the root nodule bacteria. J. Bacteriol. 37:161-85. Mechanism of symbiotic nitrogen fixation. Ergeb. Enzymforsch. 8:13-54. With E. B. Fred. The carbohydrate-nitrogen relation in legume symbiosis. J. Am. Soc. Agron. 31:497-502.
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Biographical Memoirs: Volume 61 With W. B. Sarles. Root nodule bacteria. Tabulae Biol. 17:338-67. With O. Wyss and R. H. Burris. Occurrence and significance of oxalacetic acid in plant tissues. Proc. Soc. Exp. Biol. Med. 40:372-75. 1940 With R. H. Burris. Measures of respiratory activity with resting cells. Proc. Soc. Exp. Biol. Med. 45:721-26. With C. Hurwitz. Direct estimation of biological nitrogen fixation. A gasometric method Ind. Eng. Chem. Anal. Ed. 12:31-33. With P. M. West. Biotin as a growth stimulant for the root nodule bacteria. Enzymologia 8:152-62. The Biochemistry of Symbiotic Nitrogen Fixation. Madison: University of Wisconsin Press. 302 pp. 1941 With C. J. Lind. Mechanism of biological nitrogen fixation. VIII. Carbon monoxide as an inhibitor for nitrogen fixation by red clover J. Am. Chem. Soc. 63:3511-14. With A. S. Phelps. Occurrence of hydrogenase in nitrogen-fixing organisms. Proc. Soc. Exp. Biol. Med. 47:473-76. With S. B. Lee and Orville Wyss. Mechanism of symbiotic nitrogen fixation. V. Nature of inhibition by hydrogen. J. Biol. Chem. 139:91-101. With O. Wyss, C. J. Lind, and J. B. Wilson. Mechanism of biological nitrogen fixation. VII. Molecular H2 and the pN2. function of Azotobacter. Biochem. J. 35:845-54. With O. Wyss. Mechanism of biological nitrogen fixation. VI. Inhibition of Azotobacter by hydrogen. Proc. Natl. A cad. Sci. USA 27:162-68. With O. Wyss. Factors influencing excretion of nitrogen by legumes. Soil Sci. 52:15-29. 1942 With R. H. Burris, F. J. Eppling, and H. B. Wahlin. Studies of biological nitrogen fixation with isotopic nitrogen. Soil Sci. Soc. Am. Proc. 7:258-62. With R. H. Burris. Oxidation and assimilation of glucose by the root nodule bacteria J. Cell. Comp. Physiol. 19:361-71.
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Biographical Memoirs: Volume 61 With S. B. Lee and J. B. Wilson. Mechanism of biological nitrogen fixation. X. Hydrogenase in cell-free extracts and intact cells of Azotobacter. J. Biol. Chem. 144:273-81. With C. J. Lind. Carbon monoxide inhibition of nitrogen fixation by Azotobacter. Arch. Biochem. 1:59-72. With C. J. Lind. Nitrogen fixation by Azotobacter in association with other bacteria Soil Sci. 54:105-11. With J. B. Wilson and S. B. Lee. Mechanism of biological nitrogen fixation. IX. Properties of hydrogenase in Azotobacter. J. Biol. Chem. 144:265-71. With J. B. Wilson. Biotin as a growth factor for rhizobia. J. Bacteriol. 43:329-41. With J. B. Wilson. Hydrogen in the metabolism of Azotobacter. J. Bacteriol. 44:250-51. A Symposium on Respiratory Enzymes, ed. P. W. Wilson. Madison: University of Wisconsin Press. 281 pp. With R. H. Burris and C. J. Lind. The dissociation constant in nitrogen fixation by Azotobacter. Proc. Natl. Acad. Sci. USA 28:243-50. 1943 With R. H. Burris, F. J. Eppling, and H. B. Wahlin. Detection of nitrogen fixation with isotopic nitrogen. J. Biol. Chem. 148:349-57. With C. Eisenhart. Statistical methods and control in bacteriology. Bacteriol. Rev. 7:57-137. With J. B. Wilson. Action of inhibitors on hydrogenase in Azotobacter. J. Gen. Physiol. 26:277-86. With R. H. Burris and W. B. Coffee. Hydrogenase and symbiotic nitrogen fixation. J. Biol. Chem. 147:475-81. With J. F. Hull and R. H. Burris. Competition between free and combined nitrogen in nutrition of Azotobacter Proc. Natl. Acad. Sci. USA 29:289-94. With C. J. Lind. Carbon monoxide inhibition of Azotobacter in microrespiration experiments J. Bacteriol. 45:219-32. 1944 With E. R. Ebersole and C. Guttentag. Nature of carbon monoxide inhibition of biological nitrogen fixation Arch. Biochem. 3:399-418.
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Biographical Memoirs: Volume 61 1945 With R. H. Burris. Biological nitrogen fixation. Annu. Rev. Biochem. 14:685-708. 1946 With R. H. Burris. Comparison of the metabolism of ammonia and molecular nitrogen in Azotobacter. J. Biol. Chem. 165:595-98. With R. H. Burris. Characteristics of the nitrogen-fixing enzyme system in Nostoc muscorum. Bot. Gaz. 108:254-62. With R. H. Burris. Ammonia as an intermediate in nitrogen fixation by Azotobacter. J. Bacteriol. 52:505-12. 1947 With R. H. Burris. The mechanism of biological nitrogen fixation. Bacteriol. Rev. 11:41-73. 1948 With D. M. Molnar and R. H. Burris. The effect of various gases on nitrogen fixation by Azotobacter. J. Am. Chem. Soc. 70:1713-16. 1949 With R. H. Burris and R. E. Stutz. Incorporation of isotopic carbon into compounds by biosynthesis. Bot. Gaz. 111:63-69. With E. D. Rosenblum. Fixation of isotopic nitrogen by Clostridium. J. Bacteriol. 57:413-14. With W. Segal. Hydroxylamine as a source of nitrogen for Azotobacter vinelandii. J. Bacteriol. 57:55-60. 1950 With E. S. Lindstrom and S. R. Tove. Nitrogen fixation by the green and purple sulfur bacteria. Science 112:197-98. With E. D. Rosenblum. Molecular hydrogen and nitrogen fixation by Clostridium. J. Bacteriol. 59:83-91. 1951 With L. E. Mortenson. Effect of molecular nitrogen and hydrogen on hydrogen evolution by Clostridium pasteurianum. J. Bacteriol. 62:513-14. With E. D. Rosenblum. The utilization of nitrogen in various compounds by Clostridium pasteurianum. J. Bacteriol. 61:475-80.
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Biographical Memoirs: Volume 61 With C. H. Werkman, ed. Bacterial Physiology . New York: Academic Press. 707 pp. With I. Zelitch, E. D. Rosenblum, and R. H. Burris. Isolation of the key intermediate in biological nitrogen fixation by Clostridium. J. Biol. Chem. 191:295-98. With I. Zelitch, E. D. Rosenblum, and R. H. Burris. Comparison of the metabolism of ammonia and molecular nitrogen in Clostridium. J. Bacteriol. 62:747-52. 1952 With R. H. Burris. Effect of haemoglobin and other nitrogenous compounds on the respiration on the rhizobia. Biochem. J. 51:90-96. With E. S. Lindstrom and J. W. Newton. The relationship between photosynthesis and nitrogen fixation. Proc. Natl. Acad. Sci. USA 38:392-96. With R. Repaske. Nitrous oxide inhibition of nitrogen fixation by Azotobacter. J. Am. Chem. Soc. 74:3101-3. With R. W. Stone. Respiratory activity of cell-free extracts from Azotobacter. J. Bacteriol. 63:605-17. With R. W. Stone. The effect of oxalacetate on the oxidation of succinate by Azotobacter extracts. J. Bacteriol. 63:619-22. With R. W. Stone. The incorporation of acetate in acids of the citric acid cycle by Azotobacter extracts. J. Biol. Chem. 196:221-25. The comparative biochemistry of nitrogen fixation. Adv. Enzymol. 13: 345-75. With I. Zelitch and R. H. Burris. The amino acid composition and distribution of N15 in soybean root nodules supplied N15-enriched N2. Plant Physiology 27:1-8. 1953 With L. A. Hyndman and R. H. Burris. Properties of hydrogenase from Azotobacter vinelandii. J. Bacteriol. 65:522-31. With J. W. Newton. Nitrogen fixation and photoproduction of molecular hydrogen by Thiorhodaceae. Antonie van Leeuwenhoek 19:71-7. With J. W Newton and R. H. Burris. Direct demonstration of ammonia as an intermediate in nitrogen fixation by Azotobacter. J. Biol. Chem. 204:445-51. With R. Repaske. Oxidation of intermediates of the tricarboxylic acid cycle by extracts of Azotobacter agile. Proc. Natl. Acad. Sci. USA 39:225-32.
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Biographical Memoirs: Volume 61 With R. H. Burris. Biological nitrogen fixation—A reappraisal. Annu. Rev. Microbiol. 7:415-32. 1955 Pathways in biological nitrogen fixation. In Perspectives and Horizons in Microbiology, ed. S. A. Waksman, pp. 110-20. New Brunswick, N. J.: Rutgers University Press. 1956 With A. L. Shug and P. B. Hamilton. Hydrogenase and nitrogen fixation. In Inorganic Nitrogen Metabolism, ed. W. D. McElroy and B. Glass, pp. 344-60. Baltimore, Md.: Johns Hopkins University Press. 1957 With J. H. Bruemmer, J. L. Glenn, and F. L. Crane. Electron transporting particle from Azotobacter vinelandii. J. Bacteriol. 73:113-16. With R. H. Burris. Methods for measurement of nitrogen fixation. In Methods in Enzymology, ed. S. P. Colowick and N. O. Kaplan, pp. 355-66. New York: Academic Press. On the sources of nitrogen of vegetation, etc. Bacteriol. Rev. 21:215-26. 1958 With S. Hino. Nitrogen fixation by a facultative bacillus. J. Bacteriol. 75:403-8. With R. M. Pengra. Physiology of nitrogen fixation by Aerobacter aerogenes. J. Bacteriol. 75:21-25. With M. H. Proctor. Nitrogen fixation by Gram-negative bacteria. Nature 182:891. With A. Temperli. Oxidative phosphorylation and nitrogen fixation by cell-free extracts of the Azotobacter. Experientia 14:363. Evan Pugh—Forgotten man of biological nitrogen fixation. Bacteriol. Rev. 22:143-44. Asymbiotic nitrogen fixation. In Encyclopedia of Plant Physiology, ed. W. Ruhland, pp. 9-47. New York: Springer-Verlag. 1959 With F. J. Bergersen. Spectrophotometric studies of the effects of nitrogen on soybean nodule extracts. Proc. Natl. Acad. Sci. USA 45:1641-46.
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Biographical Memoirs: Volume 61 With J. A. Bush. A non-gummy chromogenic strain of Azotobacter vinelandii. Nature 184:381. With M. H. Proctor. Nitrogen fixation by Achromobacter spp. Arch. Mikrobiol. 32:254-60. With D. W. S. Westlake. Molecular hydrogen and nitrogen fixation by Clostridium pasteurianum. Can. J. Microbiol. 5:617-20. 1960 With G. L. Bullock and A. Bush. Calcium requirements of various species of Azotobacter. Proc. Soc. Exp. Biol. Med. 105:26-30. With K. C. Schneider, C. Bradbeer, R. N. Singh, L. C. Wang, and R. H. Burris. Nitrogen fixation by cell-free preparations from microorganisms. Proc. Natl. Acad. Sci. USA 46:726-33. With A. Temperli and R. M. Pengra. Some properties of a soluble and particle-bound hydrogenase in Aerobacter aerogenes . Biochim. Biophys. Acta 38:557-58. With A. Temperli. Untersuchungen über die oxydative phosphorylierung durch Azotobacter vinelandii. Z. Physiol. Chem. 320:195-203. 1961 With F. J. Bergersen and R. H. Burris. Biochemical studies on soybean nodules. Recent Advances in Botany, pp. 589-93. With D. W. S. Westlake and A. L. Shug. The pyruvic dehydrogenase system of Clostridium pasteurianum. Can. J. Microbiol. 7:515-24. 1962 With F. H. Grau. Physiology of nitrogen fixation by Bacillus polymyxa. J. Bacteriol. 83:490-96. With A. Jackobsons and E. A. Zell. A re-investigation of the calcium requirement of Azotobacter vinelandii using purified media. Arch. Mikrobiol. 41:1-10. With D. J. D. Nicholas and M. Kobayashi. Co requirement for inorganic nitrogen metabolism in microorganisms Proc. Natl. Acad. Sci. USA 48:1537-42. With D. J. D. Nicholas, W. Heinen, G. Palmer, and H. Beinert. Use of electron paramagnetic resonance spectroscopy in investigations of functional metal components in microorganisms. Nature 196:433-36. With A. Temperli. Reactivation of succinate-cytochrome C reduc-
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Biographical Memoirs: Volume 61 tase in acetone-extracted particles of Azotobacter vinelandii . Nature 193:171. 1963 With C. Bradbeer. Inhibitors of nitrogen fixation. In Metabolic Inhibitors. A Comprehensive Treatise, ed. R. M. Hochster and J. H. Quastel, pp. 595-614. New York: Academic Press. With F. H. Grau. Hydrogenase and nitrogenase in cell-free extracts of Bacillus polymyxa. J. Bacteriol. 85:446-50. With D. J. D. Nicholas and F. J. Bergersen. Bacterial nitrogen fixation. In Yearbook of Science and Industry, pp. 138-40. New York: McGraw-Hill. With M. W. Nimeck and D. J. D. Nicholas. Nitrogen fixation in cell-free extracts of Azotobacter vinelandii prepared by lysis with phage A22 Nature 200:709. Biological nitrogen fixation—Early American style. Bacteriol. Rev. 27:369-80. 1964 With I. R. Hamilton and R. H. Burris. Hydrogenase and nitrogenase in a nitrogen-fixing bacterium. Proc. Natl. Acad. Sci. USA 52:637-41. With Y. I. Shethna, R. E. Hansen, and H. Beinert. Identification by isotopic substitution of the EPR signal at g=1.94 in a non-heme iron protein from Azotobacter. Proc. Natl. Acad. Sci. USA 52:1263-71. 1965 With I. R. Hamilton and R. H. Burris. Pyruvate metabolism by a nitrogen-fixing bacterium. Biochem. J. 96:383-89. With I. R. Hamilton, R. H. Burris, and C. H. Wang. Pyruvate metabolism, carbon dioxide assimilation, and nitrogen fixation by an Achromobacter species. J. Bacteriol. 89:647-53. With M. C. Mahl, M. A. Fife, and W. H. Ewing. Nitrogen fixation by members of the tribe Klebsielleae. J. Bacteriol. 89:1482-87. 1966 With Y. I. Shethna and H. Beinert. Purification of a non-heme iron protein and other electron transport components from Azotobacter extracts. Biochim. Biophys. Acta 113:225-34.
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Biographical Memoirs: Volume 61 1967 With R. W. Detroy, D. F. Witz, and R. A. Parejko. Complementary functioning of two components required for the reduction of N2 from four nitrogen-fixing bacteria. Science 158:526-27. With G. W. Strandberg. Molecular H2 and the pN2 function of Azotobacter. Proc. Natl. Acad. Sci. USA 58:1404-409. With D. F. Witz and R. W. Detroy. Nitrogen fixation by growing cells and cell-free extracts of the Bacillaceae. Arch. Mikrobiol. 55:369-81. 1968 With R. W. Detroy, D. F. Witz, and R. A. Parejko. Reduction of N, by complementary functioning of two components from nitrogen-fixing bacteria. Proc. Natl. Acad. Sci. USA 61:537-41. With M. C. Mahl. Nitrogen fixation by cell-free extracts of Klebsiella pneumoniae. Can. J. Microbiol. 14:33-38. With R. A. Parejko. Taxonomy of Azotomonas species. J. Bacteriol. 95:143-46. With G. W. Strandberg. Formation of the nitrogen-fixing enzyme system in Azotobacter vinelandii. Can. J. Microbiol. 14:25-31. 1969 With J. V. Dahlen and R. A. Parejko. Complementary functioning of two components from nitrogen-fixing bacteria. J. Bacteriol. 98:325-26. With C. A. Ouellette and R. H. Burris. Deoxyribonucleic acid base composition of species of Klebsiella, Azotobacter and Bacillus. Antonie van Leeuwenhoek 35:275-86. First steps in biological nitrogen fixation. Proc. R. Soc. London Ser. B 172:319-25. 1970 With R. J. Fisher. Pyruvate-supported nitrogen fixation by cell-free extracts of Bacillus polymyxa. Biochem. J. 117:1023-24. With J. Oppenheim, R. J. Fisher, and L. Marcus. Properties of a soluble nitrogenase in Azotobacter. J. Bacteiol. 101:292-96. With R. A. Parejko. Regulation of nitrogenase synthesis by Klebsiella pneumoniae. Can. J. Microbiol. 16:681-85. With M.-A. Riederer-Henderson. Nitrogen fixation by sulphate-reducing bacteria. J. G en. Microbiol. 61:27-31.
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Biographical Memoirs: Volume 61 1971 With R. A. Parejko. Kinetic studies on Klebsiella pneumoniae nitrogenase. Proc. Natl. Acad. Sci. USA 68:2016-18. The background. In The Chemistry and Biochemistry of Nitrogen Fixation, ed. J. R. Postgate, pp. 1-18. London: Plenum Press. 1972 Training a microbiologist. Annu. Rev. Microbiol. 26:1-22. 1976 With T. E. Hermann. Kinetic studies on Bacillus polymyxa nitrogenase. J. Bacteriol. 126:743-50.
Representative terms from entire chapter: