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1 February 2010 The Social Amoebae: The Biology of Cellular Slime Molds
Randy Wayne
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In The Social Amoebae, John Tyler Bonner, professor emeritus of ecology and evolutionary biology at Princeton University, writes about his beloved slime molds—organisms he has cherished for more than 60 years. While we often hear that men are from Mars and women are from Venus, slime molds are truly from Earth, and after reading Bonner's book, one feels the need, as I did, to walk outside, pick up a handful of soil, and look for a slime mold—to study, to admire, and to gain down-to-earth knowledge and insight into the fundamental processes that make all life on Earth possible.

Bonner describes the stages and transformations that occur in the life cycles of the cellular slime molds. He explains how these molds have provided researchers with many opportunities to conduct meaningful studies, using simple equipment, that enabled us to understand general biological problems, including the differentiation of cells, functional redundancy, cell motility, cell signaling, self organization, and the development of multicellularity. The life cycle of a cellular slime mold begins when a spore germinates to form a single-celled amoeba that feeds on bacteria. As long as there is plenty of food, the amoebae divide and live as single-celled organisms. As the bacterial food source becomes depleted, however, the amoebae aggregate to form a multicellular slug in response to a chemical signal from a single group of cells or a single founder cell. By sensing light, thermal or gaseous gradients, the multicellular slug then migrates to find an appropriate location for fruiting so that the spores can be dispersed by animals living in the soil. Bonner shares with us that “When one arrives in the laboratory in the morning, the slugs in every culture dish will all be pointing towards the window.” Upon finding a suitable location, the cells of the slug transform into stalk cells or spore cells as they form the fruiting body, or sorocarp. Information on cellular slime molds obtained from slowly publishing individual craftspeople using inexpensive equipment is currently being supplemented by information obtained by rapidly publishing, multinational consortia using expensive molecular techniques.

Realizing that the number of publications on cellular slime molds had risen from an average of 3.4 per year to an average of 224 per year over the course of his career, Bonner decided to write The Social Amoebae as an exercise to place the “factual bricks” created by the growing literature on the molecular biology of cellular slime molds into a coherent “mansion,” so that the curious layperson could gain a complete picture of the biology of slime molds. In so doing, I believe he found that the new molecular facts had such a short half life and rapid turnover rate that he wrote The Social Amoebae so practicing cellular slime mold biologists would plan and analyze their work with a “more generalized biological point of view” to guarantee that “the lessons learned would last for some time.”

The book is extremely well written. In fact, the rhetorical style reminds me of the funeral oration given by Mark Antony in Julius Caesar. In the introduction of The Social Amoebae, Bonner writes: “The molecular genetics of the developmental biology of D. discoidium (which was now simply called Dictyostelium, reflecting its newfound status as a model organism) became central. The most recent high point in this program has been the sequencing of its entire genome: now it is possible to find out how many genes we share with a slime mold. The result is that our insights and understanding of the development of Dictyostelium has vastly increased.” Although Bonner acknowledges “that it is inconceivable to study the biology today of any organism without genetics and molecular biology,” he warns us in the chapter titled “The Future” that “we are looking at finer and finer details at the risk of losing the big picture,” and “it is increasingly obvious that knowing all the genes identified in an organism does not really tell us how the organism is constructed or how it develops. Again, it is a pile of bricks and the architect's plans are hidden from us.”

Another motivation for writing The Social Amoebae came from Bonner's realization that research on the nonmolecular biological aspects of cellular slime molds had been overshadowed by the number of workers and publications in molecular developmental biology. In order to illuminate the aspects of cellular slime mold biology that have been overshadowed, Bonner gives “equal time to their evolution, their ecology, their behavior, both as single amoeba and as cell masses, and their development.”

To me, “equal time” to general biology is a euphemism used by Bonner to remind biologists that there are many valid approaches to study the cellular slime molds besides the reductionist approach of doing molecular biology (or “omics”) for its own sake, without extensive integration with the broad foundation of general knowledge of slime mold biology—and, moreover, that exclusively using such a reductionist approach may result in obtaining data that are devoid of biological information, or even worse, data that are misleading. For example, Bonner discusses the cellular slime mold family tree generated by Schaap and colleagues (2006) based on the sequence of two genes, SSU rDNA and α-tubulin. Schaap and colleagues separated 75 species of cellular slime molds into four major clades, none of which corresponds to the three traditional genera. According to this tree, the two whorled Polysphondylium species, Polysphondylium violaceum and Polysphondylium palladium, both of which initiate aggregation with a single “founder cell” instead of a group of cells, and both of which use the dipeptide glorin as opposed to cyclic AMP as an intercellular signaling agent, are not closely related to each other.

Bonner is skeptical of the conclusion that this suite of characters arose independently in the two species, and cautions us that the phylogenetic tree deduced from modern molecular research “is based on only two genes, and it will be important to examine their differences involving more genes.” While the complete revision of dictyostelid taxonomy called for by Schaap and colleagues may be premature, molecular phylogenies on the basis of many and thoughtfully chosen genes may provide profound insights not only for cellular slime mold evolution but also for all of biology. For example, the evolution of the cAMP (cyclic adenosine monophosphate) signaling system can be elucidated by applying the molecular tools used by Alvarez-Curto and colleagues (2005) to study the cAMP receptors to the study of adenylate cyclases and phosphodiesterases. Bonner suggests that by using the genes that are involved in processes that characterize the unique biology of cellular slime molds in future phylogenies, one will not only obtain a more biologically meaningful phylogeny of cellular slime molds but also insight into the cAMP signaling system.

The book is neither fashionable nor trendy, but The Social Amoebae is an enlightening and enjoyable read for the layperson and professional who would like to share in the biological insight and knowledge gained by John Tyler Bonner as a result of his lifelong relationship with cellular slime molds. To summarize, I will conclude with a quote from Mark Antony's oration: “Here is the will.... He has left you all his walks, his private arbors and newplanted orchards—he has left them all to you.” And to paraphrase Mark Antony, “Here was a biologist! When comes another?”

References cited

1.

E Avarez-Curto , DE Rozen , AV Ritchie , Fouquet , SL Baldauf , P. Schaap 2005. Evolutionary origin of cAMP-based chemoattraction in the social amoebae. Proceedings of the National Academy of Sciences 102: 6385–6390. Google Scholar

2.

P Schapp , et al. 2006. Molecular phylogeny and evolution of morphology in the social amoebas. Science 314: 661–663. Google Scholar
Randy Wayne "The Social Amoebae: The Biology of Cellular Slime Molds," BioScience 60(2), 156-157, (1 February 2010). https://doi.org/10.1525/bio.2010.60.2.11
Published: 1 February 2010
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