Perspectives in Biology and Medicine

EXTREME PLEOMORPHISM AND THE BACTERIAL LIFE CYCLE: A FORGOTTEN CONTROVERSY MILTON WAINWRIGHT* The first 40 years of this century witnessed bacteriologists involved in a debate which was fought with an intensity not seen since the arguments over spontaneous generation conducted during the last quarter of the 19th century. This now long-forgotten controversy concerned the question of whether or not bacteria exhibit extreme pleomorphism and go through complex life cycles. The term pleomorphismsvzs. used to refer to the supposed ability of bacteria to change shape dramatically, or to exist in a number of extreme morphological forms. Thus it was believed that bacteria could change from a single coccoid to complex filamentous forms and vice versa. In addition, rather than reproducing by single division, bacteria were thought to undergo complex life cycles involving single cells, spore, filaments , and ultra-filterable forms. The debate split microbiologists into two opposing schools: the monomorphists and the pleomorphists. The monomorphists finally triumphed, but as we shall see, even today reports continue to appear apparently showing that bacteria exhibit extreme morphological variations and undergo complex life cycles. Nearly all modern microbiologists belong to the monomorphic school; that is, they accept that, apart from minor variation, each bacterial cell is derived from a previously existing cell of practically the same size and shape. Cocci generally beget cocci, and rods give rise to rods. The monomorphist view, stressed byVirchow, Cohn, and Koch, is that by binary fission most bacteria divide transversely to produce two new cells which eventually achieve the same size and morphology of the original. In the same way, a single spore germinates to give rise to a vegetative cell essentially the same as the cell from which the spore originated. Exceptions to this rule are accepted in certain so-called higher bacteria, including some actinomycetes . Simple bacteria, on the other hand, are generally regarded as show- *Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, SlO 2UH, United Kingdom.© 1997 by The University of Chicago. All rights reserved. 0031-5982/97/3904-0981$01.00 •ectives in Biology and Medicine, 40, 3 ¦ Spring 1997 407 ing only occasional, slight morphological variation. This view of bacterial morphology and growth is so enshrined in our view of these organisms that we rarely bother to think about it. Despite this, there are a small number of latter-day heretics who continue to provide evidence which, they claim, supports the pleomorphist heresy. The Historical Literature on Extreme Pleomorphism and the Bacterial Growth Cycle The original pleomorphists were particularly active during the first three decades of this century. The basic tenet of their belief was that even common bacteria showed complex life cycles which often included a frequently pathogenic, filterable, or hidden phase [I]. Some even suggested that bacteria are merely rudimentary components of the fungal life cycle. The principal proponents of pleomorphism, such as Almquist, Bergstrand, Hort, Lohnis, Mellon, and Enderlein, have largely been forgotten. However, even renowned microbiologists like Ferdinand Cohn published evidence in support of extreme pleomorphism. Similarly, the eminent American bacteriologist , Theobald Smith, isolated a bacterium which apparenüy occurred in three forms: a bacillus, a coccus with an endospore or arthrospore, and a conglomeration of all three [2]. The most thorough account of the pleomorphist case is given in the monograph by F. Lohnis entitled Studies upon the Life Cycle ofBacteria [3]. If the weight of proffered evidence alone had been the sole criterion used to establish proof, then this book on its own would probably have given the argument to the pleomorphists. By 1928, in an article on morphology published in the monograph The NewerKnowledge ofBacteriology and Immunology, Clark could state that "bacteria , even amongst the Eubacteriales, do at times reproduce by means other than equal fission seems to me to be definitely proved" [4]. He quotes the work of Hort, who showed that under adverse conditions, colon-typhoid bacteria reproduce by budding, by producing Y-shaped and large aberrant forms and deeply staining granules which can be filterable [5, 6]. Hort went on to describe how these irregular bodies reproduced actively and so were not examples of so-called involution forms, a term used by the monomorphists to suggest that what the...