Rebuttal: Problems with “Procaryote”

Abstract

Even though the procaryote-eucaryote classification is based upon cellular structure and, in principle, impervious to phylogeny, the eucaryotes are monophyletic, so this scheme is coincidentally consistent with a phylogenetic classification. Nevertheless, as Pace (2) points out, the procaryotes are probably paraphyletic. This is not a flaw in the classification but one of the components in its definition. While phylogeny is extremely informative for classification, it is insufficient alone, and additional information is required for evaluation of the importance of the different evolutionary events which led to the creation of modern organisms. For instance, the bacteria are composed of many very distinct phyla and encompass organisms as dissimilar as the enteric bacteria, cyanobacteria, and Planctomycetes. They are unified within a single group, in recognition of the shared differences from the archaea and the importance placed upon those differences. If these differences were perceived to be small, the procaryotes might be composed of numerous phyla without recognition of domains at all. Therefore, recognition of the domain Bacteria is based on both our evaluation of the biological properties of these organisms and our perception of their phylogeny. During the preparation of this article, a reviewer posed the critical question. Which classification is a better predictor of an organism’s properties, the cellular classification of procaryotic or the phylogenetic classification of archaeal or bacterial? Both are needed. Certainly, phylogeny predicts some properties well, such as the type of RNA polymerase or cellular lipid. However, being a procaryote predicts other things well, such as metabolism, bioenergetics, and life-style. Based upon gene trees, evolutionary clocks, and the fossil record, the ancestor of the eucaryotes almost certainly possessed a procaryotic cellular structure. Hence, it was a procaryote. While most of the evidence about ancient life was not available at the time the terminology was proposed, the prefix “pro” has proven fortuitously apt. Similarly, phylogenetic trees of the rRNAs and other highly conserved genes demonstrate that all modern organisms share a common origin. While the weight of evidence suggests that the root of the universal tree is within the procaryotes, this point has not been unambiguously resolved (1). If the root turns out to be on the lineage leading to the modern eucaryotes, then the discussion of the validity of the procaryotes will be moot. Most importantly, gene trees are not equivalent to organismal trees. The root of the rRNA gene tree provides no evidence for the primordial origin of the nuclear component eucaryotes because the same topology would be expected of the gene tree regardless of whether it was derived from a primordial or an archaeal lineage. Lastly, the evolutionary events that separate eucaryotes from archaea are also sufficient to distinguish them from the bacteria, from which their organelles were derived. In fact, it is our perception of their importance that is the basis for the procaryote-eucaryote dichotomy. Even if the procaryotes were defined solely by negative characteristics, this would not be a fatal flaw in the classification. Examples of robust classifications based upon negative characteristics include anaerobe, absolute zero, and prime number. Lastly, while the alternative term “microbe” has proven useful in some circumstances, its ambiguity is problematic. What size limit defines the microbes? Are the large bacteria, such as Thiomargarita and the multicellular cyanobacteria, microbes? The Armillaria fungi are among the largest organisms on earth (3). Are they microbes? Size is an important biological characteristic, but is it sufficient to neglect the enormous structural, molecular, physiological, and ecological features that unite the procaryotes?