➤ Arthur T. Henrici (1889-1943), who began his career in medicine, is an unsung hero of microbiology, whose interests shifted to basic physiology and microbial ecology during his brief but distinguished career.
➤ Henrici contributed several key insights in basic microbiology-for example, relating changes in cell size to growth rate and discovering biofilms.
➤ Henrici's studies helped to arrive at a compromise between the extreme views of monomorphism and pleomorphism.
➤ Henrici helped to open the new field of research of freshwater microbial ecology by conducting field studies of microorganisms from Minnesota lakes.
➤ His freshwater studies uncovered species belonging to the genus Caulobacter, one of which is now used widely for studying morphogenesis.
Arthur T. Henrici, a fascinating man, is an unsung hero of microbiology. Born in Economy, Pa., in 1889, Henrici graduated from medical school at the University of Pittsburgh in 1911 at the head of his class. He worked locally as a pathologist at the St. Francis Hospital until 1913, when he moved to Minnesota to begin his long tenure on the bacteriology faculty at the University of Minnesota-remaining there until his untimely death in 1943 at the age of 54.
Life for him was a series of challenges to meet and overcome before moving to the next. Thus, he became a photographer, built his own camera, won a prize for bird photography, and then sold the camera. Similarly, after becoming an expert rifleman and winning a national competition, he sold the rifle; later, he became a virtuosic flutist but then sold his flute. When he built a radio, the physics department invited him to teach a course on radios, but he declined. When nearly everyone owned a radio, he sold his. He became an artist, developed a technique for steel etching, won an international prize and then presented his press to a museum; one of his watercolors hangs in the Henrici Library at the University of Minnesota.
The one challenge he persisted with through all of his brief life was microbiology. His scholarly achievements were diverse, ranging from medical microbiology to a massive review on yeasts to freshwater microbiology and to a masterly, seminal monograph on the relationship between growth rate and morphogenesis in bacteria. He was a consummate teacher and writer, and his scholarly works include the monograph Molds, Yeasts, and Actinomycetes and the textbook The Biology of Bacteria, which went through three editions.
In 1917 Henrici was promoted to Assistant Professor in Bacteriology and Public Health. That same year he interrupted his academic career by enlisting in the U.S. Army to serve with the Army Medical Corps in France until the 1918 armistice ended the war in Europe. He then returned to Minnesota and resumed what became a distinguished career in research and teaching. In 1939 he was elected President of the Society of American Bacteriologists, which later became ASM.
The early part of Henrici's career reflected his training as a physician, and his fırst 12 publications, from 1913 to 1923, involved research in oral and medical microbiology. However, his interests shifted from medical to more fundamental properties of microorganisms beginning in 1922, when he wrote the fırst in a groundbreaking series of papers on the relationship of the shape of bacteria to their rate of growth. His interests soon expanded from bacteriology to include the study of yeasts, fungi, and actinomycetes, which were then considered intermediate between bacteria and fungi. Near the end of his short life, he became interested in freshwater microbiology, and his series of published papers transformed that fıeld.
Our departmental library at the University of Minnesota, named The Henrici Library, serves as a repository of his books, monographs, reprints, many of his original photographs, and an extensive collection of slides from his freshwater bacteriology research.
An Early Research Focus for Henrici: the Shapes of Cells
What Henrici called the "new pleomorphism" catalyzed his breaking from medical and oral microbiology to confront new research challenges in fundamental microbiology. Monomorphism and the techniques of pure culture championed by Ferdinand Cohn and Robert Koch in the late 19th century dominated microbiology for the next 50 years. Their approach was a useful antidote to Karl von Naegeli's doctrine of pleomorphism, which held that one could view all bacteria as being members of only one or two groups, which manifested a variety of morphological shapes as part of a series of complex life cycles.
Dogma has a price, however, and the blind acceptance of the Cohn-Koch doctrine of the constancy of cell forms stood in the way of microbiologists examining the real problem of morphological variation in bacteria. Hence, pleomorphism resurfaced in the early 20th century, largely thanks to Felix Lohnis, who studied the microcysts of Azotobacter.He held that most bacteria exhibit life cycles that account for the variety of shapes viewed in complex bacterial populations.
Henrici was cautious in his view of the new pleomorphism, noting:
". . . this movement has within it that danger inherent in all revolutionary movements, the tendency to go too far in the opposite direction. It does not necessarily follow that because Koch was wrong, Naegeli was right. . . ."
From 1922 to 1929, he examined morphological variations as a function of growth cycles in Bacillus megatherium (sic), Vibrio cholerae, Bacterium coli, and a coryneform bacillus. That work led to 10 publications and culminated in his monograph, Morphologic Variation and the Rate of Growth of Bacteria. Henrici was insistent that contributions to the then-current debate about bacterial life cycles be based on data and not philosophical meanderings. Henrici was unsparing in his criticism of one contemporary:
"The impression that the work is philosophical rather than the result of laboratory observation is supported by the fact that the author is a zoologist. . . ."
More generally, Henrici insisted on systematic experiments, continuous observation of the sequences of changes within cultured bacteria, and relying on data to draw conclusions. He deplored those who broke those rules, castigating anyone who neglected to follow the details of what microorganisms might do. Thus, he wrote,
"[C]ultures are examined today and then set in the icebox (!) for weeks or months at the end of which time they are found to have undergone a transformation."
Several Enduring Insights from Henrici's Research
His work resulted in several important insights. The fırst was that the size of the cells of Bacterium coli was a function of the stage of the growth cycle at which the cells were being measured. He carefully determined the sizes of such cells by calculating the ratio of cell length to volume for hundreds of cells viewed in magnifıed photomicrographs (Fig. 1).
Another insight was that when the growth rate of a bacterial culture is varied by limiting nutrients, cell size increases as a function of growth rate. For instance, Vibrio cholerae reacts in this fashion. While measuring bacterial cell size, he also determined their shapes by using what he called a curvature index, the ratio of the length of the cell to the distance between its tips. These results are beautifully represented in a threedimensional graph plotting growth rate, cell shape and cell size of V. cholerae as functions of time during a normal growth cycle. (Fig. 2).
Yet another insight related to the larger debate over pleomorphism versus monomorphism. Henrici held that neither of the polarized opposite positions accurately characterize bacteria. Moreover, as happens often with complex phenomena, the dialectic was resolved by synthesizing the two positions. He concluded that the appearance in a bacterial culture of a variety of morphological shapes was neither an invariable reflection of a complex life cycle as held by the pleomorphists, nor of dead and dying cells as held by the monomorphists. Rather, as bacterial cells move through their growth cycle, they manifest regular changes in size and shape as a function of growth and division. In his own words:
"In this work I shall show that, contrary to the orthodox teaching, the cells of bacteria are constantly changing in size and form and structure; but that instead of these changes occurring in a haphazard or meaningless fashion, or instead of being phases in a rather vague and complex life cycle, they occur with great regularity and are governed by simple laws which, after more data have been accumulated and analyzed, may probably be very precisely formulated."
Indeed, 30 years later, Moselio Schaechter, Niel Ole Kjeldgaard, and Ole Maaloe precisely formulated those terms in a way that redirected research for those studying bacterial growth physiology.
Microbial Ecology in the Land of 10,000 Lakes
As a microbiologist in Minnesota, "the Land of 10,000 Lakes," Henrici naturally developed an interest in freshwater microbial ecology.
"The vast amount of labor that has been spent on water bacteria has been carried on almost exclusively from the standpoint of sanitation and is almost worthless from the standpoint of ecology," he wrote.
Henrici realized that the census of bacteria in any environment, as determined by conventional culture technology, reported only a small fraction of the number and types of bacteria present in each sample and place. In addition, the diversity of morphological types that were isolated from freshwater did not reflect what Henrici intuitively believed was characteristic of this or any other ecological niche. His fındings were timely, tracking the work of Sergei Winogradsky and other microbiologists who were also moving toward a more rational study of microbes in natural environments.
Henrici noticed that the walls of an aquarium in his lab became coated with a thick growth of algae. Amicroscope slide placed in the aquarium likewise developed such growth. However, when the slide was stained it also revealed a coating of bacteria, many of which were of unusual morphology. They also appeared as microcolonies, which suggested to Henrici that they were not only attaching to the glass surface but were also growing on it. He called them "benthic"-what we now know as biofılms-and distinguished them from the planktonic cells, floating freely, which he suggested were released by forces acting on the slide surface or were part of the life cycle of the organism.
He then shifted his attentions to lakes and devised a simple technique in which glass slides were attached to a wire, anchored to the bottom of the lake while hung from floats easily visible so they would not be snagged by passing boats. These devices also carried signs requesting that curious passers-by leave them undisturbed. The results from these studies were extraordinary. His fırst of fıve papers on the microbial ecology of lakes provided a glimpse of a variety of strange fılamentous and stalked bacteria that appeared on some of those suspended slides.
Early studies of Caulobacter
In his second paper of this series, Henrici described these organisms in more detail, but focused on the newly recognized group of stalked bacteria that he described as belonging to the order Caulobacteriales (sic), based on the Greek caulos, a stalk. The new order comprised a number of families that now, based on molecular phylogenetic analysis contains only the family Caulobacteraceae. It includes the genus Caulobacter, which Jeanne Poindexter more fully described 29 years later in her magisterial monograph in Bacteriological Reviews. Since then, Caulobacter became a favorite microorganism for studying development and morphogenesis.
The various stalked bacteria comprising the Caulobacteriales (sic) and the genus Caulobacter include two budding bacterial genera that Henrici and his collaborator Delia Johnson named "Blastocaulis" and "Pasteuria" (Fig. 3). These bacteria are members of the Planctomycetes, according to James Staley at the University of Washington and his collaborators, who isolated them in pure culture during the 1970s. Unlike Caulobacter and related forms that are members of the phylum Proteobacteria, the Planctomycetes comprise an entirely separate phylum within the Bacteria. The name Planctomycetes was given to them because the Hungarian biologist, N. Gimesi, who identifıed them in lakes in 1924, thought they were planktonic fungi. Henrici and Johnson, who were unaware of Gimesi's work, correctly concluded that they were bacteria.
Henrici and Johnson illustrated and photographed an organism that they named the "fusiform" Caulobacter, which is now in the genus Prosthecobacter. Staley's group placed this genus in a separate bacterial phylum, the Verrucomicrobia, and it is the only known bacterial genus that contains both alpha and beta homologs for tubulin genes, which are found in all members of the Eukarya.
The remaining three papers in the freshwater series described Henrici's attempts to quantify these bacteria and to describe their seasonal fluctuations. However, in another paper, Henrici acknowledged the limitations of the submerged slide technique and returned, almost reluctantly, to using culture methods, albeit with the hope that they would someday support the growth of unusual organisms he detected but could not grow in the lab. Doubtless, he would be delighted, if not a bit cautious, to learn how metagenomic techniques are being used currently to meet just such research challenges.
In delving into freshwater microbiology, Henrici opened our eyes to the remarkable morphological diversity of bacteria from such settings, particularly to those many species that resist cultivation. He also fırst described biofılms- now a burgeoning fıeld in biology. Sadly, his underappreciated career was cut short by his untimely death at the age of 54. Who knows where his talents might have taken him?
Martin Dworkin is Emeritus Professor in the Department of Microbiology, University of Minnesota.
I wish to acknowledge the help of James Staley and Tim Brickman.
Henrici, A. T. 1928. Morphologic variation and the rate of growth of bacteria. Charles C. Thomas, Publisher, Springfıeld, Ill., and Baltimore, Md.
Henrici, A.T. 1933. Studies of freshwater bacteria. I. A direct microscopic technique. J. Bacteriol. 25:277- 286.
Henrici, A. T., and D. E. Johnson. 1935. Studies of freshwater bacteria. II. Stalked bacteria, a new order of Schizomycetes. J. Bacteriol. 30:61-92.