As microbiology advances in a number of directions, our perspectives
on what has gone before and where it is going are bound to change Moselio Schaechter
n 1962, Thomas Kuhn wrote a book of unhurried, yet the total flux contributes mean-
I seminal importance, The Structure of ingfully to geochemical activities. In the oceans,
Scientific Revolution, wherein he intro- microbes carry out about as much photosynthe- duced the concept of “paradigm shift.” sis as all land plants combined. Prokaryotic and Kuhn proposed that science advances eukaryotic microbes share the work, perhaps through a “series of peaceful interludes punctu- equally. Metagenomic techniques even allow ated by intellectually violent revolutions,” revo- some measure of a census of the microbes lutions in which “one conceptual world view present in many habitats. We can securely con- is replaced by another.” Paradigm shifts occur tend that geologic and atmospheric transactions rapidly; other significant insights take their time cannot be considered without including the ac- in developing and are the stuff of “regular” tivities of microbes. Both quantitatively and science. Borrowing from the language of influ- qualitatively, much of the planet’s metabolism is enza virology, I will call the latter “paradigm microbial. And I haven’t even mentioned the drifts.” How do these concepts apply to the viruses! microbial sciences? Evolution. Two radical findings characterize A paradigm shift, in the Kuhnian view, must the modern view of evolution: the existence of have some of these attributes: unprecedented, three domains of life and the lateral transfer of open-ended, broad, simple, and fruitful. The genes between species. Both are fundamental definition does not readily lend itself to quanti- concepts, and both arose abruptly. Conceptu- tative analysis, and I will use a personal reading ally, both leave key questions open. Thus, what of Kuhn’s terms. I present here examples of is the origin of the three domains? Discussions what in my mind constitute paradigm shifts in abound, especially about the ancestry of eukary- microbiology. Each of them can be reduced to a otic cells. Of equal concern is the extent and Moselio Schaechter generalization that is both gracefully simple and importance of lateral gene transfer. To what is Chair of the Mi- exceedingly far-reaching. I realize that making degree does it inconvenience the very concept of crobe Editorial such choices may be audacious, but it is meant the Tree of Life? Or is it mainly relevant to the Board and Distin- to be merely a personal statement. My purpose lower taxa? Strongly held views exist on all guished Professor, here is primarily to elicit discussion. these questions. Are today’s tools adequate to Emeritus, Tufts Uni- The Planetary Prevalence of Microbes. It has resolve them? Will more genome sequencing versity School of Medicine, Boston, been known for centuries that massive rock and informatics analysis further our under- Mass.; Adjunct Pro- deposits such as limestone, biogenic silica, and standing of how microbes, and indeed all of life, fessor Emeritus, coal are of biological origin, much of it micro- have evolved? Or must we await a new method- Department of Biol- bial in nature. Still, it came as a surprise some ology? ogy, San Diego years ago when it was calculated that the Earth’s Microbial Sociology (or Sociomicrobiology). State University, extant biomass is hugely microbial, the mi- For most of the history of bacteriology, bacteria San Diego, Calif.; crobes perhaps comprising as much as half the were thought to perform as individuals, with and Visiting total weight of living things. Much of this enor- only a few significant interactions between Scholar, University mous global cargo is found in the underground them. The few celebrated instances of collective of California at San water occupying the spaces within the rocks. behavior, such as seen in certain differentiating Diego. Here, metabolism is thought to be slow and bacteria, were considered to be special cases. We
538 Y Microbe / Volume 4, Number 12, 2009
now know that bacteria and archaea build com- are distinctly work in progress. I have no doubt plex and interactive communities, the result of but that eventually they will lead to important intricate conversations between them. But be- generalizations, but not quite yet. This view yond that, even “planktonic” prokaryotic cells does not diminish their grandeur and luster. I communicate with one another. Much like in- present one example. sects, they use specific chemical compounds as Microbial Cell Structure. Ours is the Age of their community organizers. These act to turn Imaging. Biology has rendezvoused with its vi- on and off genes, direct the making of biofilms, sual origins. For much of its recent history, the and trigger a response to inimical influences chemical way of looking at things biological such as antibiotics. Generally speaking, bacteria prevailed. Enormously contributory as it was, and archaea act like the social insects. They are visual it was not. How things have changed! indeed “superorganisms.” Not only must we Now, every aspect of biology has benefited from treat microbes with greater regard in general, we methodological developments in microscopy, may also presume that the behavior of all living from the ability to visualize single molecules, things evolved from that of the “simple forms of often within living cells, to the discovery of life.” bacterial cytoskeleton-like structures, to the Cellular Microbiology. (I consider this a chance to “crawl” inside cells to see what they thorny term, as all microbiology is cellular, are made of. Optical tweezers technology per- but it seems to have traction, so I will use it mits the study of single molecules in action— here.) Previously, hosts and symbionts, bene- polymerizing, stretching, pulling, twisting. The ficial or otherwise, were believed to go their optical microscope is now transcending the bar- own separate way. The exception to this had rier of physical resolution, thanks to an array always been the viruses, while pathogenic bac- of fancy methods with acronyms such as SI, teria, fungi, and protists were thought not to PALM, STORM. The electron microscope is not have such a close interdependence with their left out, with progress in cryotomography and hosts. We now know that hosts and parasites other techniques, and neither are various scan- interact extensively at a molecular level, each ning probe microscopes. New views are gradu- using molecular and structural constituents of ally replacing old ones with regard to the behav- the other for their own apparent purposes. ior of individual molecules and the structure of The kinds of mutual appropriations and em- cells and viruses. But, despite all these magnifi- bezzlements of course differ between specific cent development, few generalizations are yet pairings, reflecting the skills and competency possible in this field. of each member, but, in each case, the give and Now, how about the advances in such areas take is extensive and has profound conse- quence. Our thinking has shifted from viewing as the regulation of gene expression, the animal symbiosis and parasitism in terms of pairs of microbiome, the evolution of symbioses, and organisms engaged in a complex choreogra- many, many more? I would like to leave their phy to a more unitary view in which the two status as being open to discussion. You might constitute a new whole. add to this list or argue about individual choices. Surely, readers will want to add to or subtract A suitable venue may be our blog, Small Things from this list of paradigm shifts since, as I im- Considered. Whether my choice of shifts and plied above, there is considerable room for opin- drifts matches yours or not, no matter. Let us ions. Here I will posit that many of the most rejoice in living at a time when the list of micro- exciting current developments in microbiology biological nominees is growing at such a rapid qualify rather as paradigm drifts because they pace.