JOURNAL OF BACTERIOLOGY, Jan. 1994, p. 1-6 Vol. 176, No. 1 0021-9193/94/$04.00+ Copyright 1994, American Society for Microbiology
MINIREVIEW The Winds of (Evolutionary) Change: Breathing New Life into Microbiology GARY J. OLSEN,'* CARL R. WOESE,1 AND ROSS OVERBEEK2 Department ofMicrobiology, University of Illinois, Urbana, Illinois 61801, and Mathematics and Computer Science Division, Argonne National Laboratory, Argonne, Illinois 60439-48012
Of all the spectacular changes that have transformed biology a bacterium"' (28). The problem with and the pernicious over the last several decades, the least touted, but ultimately nature of this dichotomy lay in the fact that the prokaryote was one of the most profound is that now under way in microbiol- initially defined negatively, in cytological terms. In other ogy. It is not simply that we are coming to see microbiology per words, prokaryotes lacked this or that feature characteristic of se in a new light but that we are coming to appreciate the the eukaryotic cell: even oil drops, or coacervates, could fit central roles microorganisms play in shaping the past and such a negative definition. Any virtue in the prokaryote- present environments of Earth and the nature of all life on this eukaryote dichotomy lay in what it could contribute to an planet. Because each organism is the product of its history, a understanding of the eukaryote, which might have evolved knowledge of phylogenetic relationships-of common evolu- through "prokaryotic" stages. With repetition (as catechism) tionary histories-is essential to understanding the nature of the prokaryote-eukaryote dichotomy served only to make any organism. Thus, it is unavoidable that evolution (a field microbiologists easily accept their near total ignorance of the much neglected in this molecular era) must be the conceptual relationships among prokaryotes; they were even dulled to the heart of biology; all extant life traces back to common ances- fact-one of the great challenges of today-that they did not in tors, and the earliest ancestors were microorganisms. the slightest understand the relationship between the pro- Despite considerable effort, microbiologists were never able karyote and the eukaryote. The matter of relationships among to determine the phylogenetic relationships among pro- bacteria had boiled down to "if it isn't a eukaryote, it's a karyotes (29). Not only did they ultimately give up on this prokaryote," and to understand prokaryotes, we had only to problem, but some went so far as to declare it unsolvable (27, determine how Escherichia coli differs from the eukaryotes. 28). By the 1960s most microbiologists concerned themselves This was no invitation to creative thought, no unifying biolog- little and cared even less about relationships among microor- ical principle. This eukaryote-prokaryote dichotomy was a ganisms. As a consequence, microbiology was not structured barrier that separated prokaryotic microbiology from eukary- about a "natural," phylogenetically valid system of classifica- otic microbiology. tion. Lacking this essential evolutionary touchstone, microbi- This myopic view of microbiology failed to appreciate not in an incomplete, if not distorted, way. ology developed only how important the problem of microbial relationships was Having no natural center, microbiology fissioned into sepa- but that an intractable problem today may not be so tomorro&. rate disciplines pursuing (seemingly) divergent goals. The isolation and determinative Molecular sequences had been used to determine evolutionary traditional pursuits of organism the 1950s, and Zuckerkandl and Pauling's as side relationships since classification (i.e., naming) continued, did the applied his- of microbiology (medical, industrial, etc.). However, the disci- seminal article "Molecules as documents of evolutionary made the case most compellingly in 1965 (36). Yet the plines that came to dominate and define the field reflected the tory" record shows that microbiology-the biological science most in new molecular outlook: i.e., the detailed genetics of particular effectively blind to the significance and potential of organisms, the comprehensive molecular biology of a "repre- need-was and the detailed biochemistry of this or these approaches. sentative" prokaryote, end of the 1970s however, the situation changed that metabolic pathway. Microbial ecology was a weak, in a At the rRNA sequences had been shown to provide a sense immature, discipline, stymied not only by the lack of a dramatically. (e.g., 8). No matter that on the natural system but also by the requirement that a species be key to prokaryote phylogeny levels the prokaryotes did not pro- cultured and characterized before its role in a microbial cellular and physiological community could be explored. vide characteristics that permitted their reliable phylogenetic were more than sufficient to do so. By The most profound symptom of microbiology's unfortunate ordering; their rRNAs the as the rRNA-based phylogeny of prokaryotes condition was its reliance on the prokaryote-eukaryote dichot- early 1980s, began to emerge, microbiologists began (albeit extremely omy as a phylogenetic crutch, something that replaced any understanding of microbial relationships: it represented slowly) reawakening to the importance of knowing microbial useful phylogenies. microbiology's ". . . only hope of ... formulating a 'concept of The folly of having taken all prokaryotes to be of a kind was dramatically revealed by the totally unanticipated discovery of Archaea called archaebacteria), a group of * Corresponding author. Mailing address: Department of Microbi- the (originally ology, University of Illinois, 131 Burrill Hall, 407 South Goodwin Ave., prokaryotes that, if anything, is more closely related to Eucarya Urbana, IL 61801. Phone: (217) 244-0616. Fax: (217) 244-6697. (eukaryotes) than to the other prokaryotes, the (true) Bacteria Electronic mail address: [email protected]. (11, 13, 32, 34). Even then, the power of the eukaryote- 2 MINIREVIEW J. BAcrERIOL. prokaryote dichotomy as phylogenetic dogma was strikingly bacteria contain photosynthetic species, and each of the five demonstrated by the fact that the majority of microbiologists manifests a distinct type of (chlorophyll-based) photosynthesis. (and biologists) were initially unable to accept that there could The cyanobacteria have also given rise to the chloroplasts, be two types of prokaryotes that are not specifically related to which are the basis for all photosynthesis found in eukaryotes. one another. (An amazing aspect of the history is that [at the It would appear that photosynthetic metabolism is the ultimate time] a biologist would most likely have agreed that the nuclear evolutionary source of much of the metabolic diversity found genome came from a "prokaryote-like" ancestor, i.e., the most among the bacteria, which in turn is the source of key recent common ancestor of eukaryotes and bacteria. After all, biochemistries (e.g., photosynthesis and respiration) among this is inherent in the prokaryote-eukaryote dichotomy. Yet the eukaryotes. the idea that specific prokaryotic relatives of the eukaryotes The molecular revolution in microbiology means much more have persisted to the present was anathema. As best as we can than just a new taxonomy. For example, microbial ecology is tell, these noneukaryote descendants do exist; we call them being reborn. The remarkable insight of Norman Pace that Archaea. However, the nature of biologist's objections was not organisms can be (phylogenetically) identified directly in their monolithic. For example, Margulis and Schwartz [19] sug- niches-through a combination of rRNA gene cloning and gested that the origin of [most of] the nuclear genes was indeed sequencing, and the design and use of rRNA-directed "phylo- a specific group of [true] bacteria, the "aphagramabacteria." genetic stains"-has sparked a revolution in that discipline (5, This view had the merit of proposing that some prokaryotes 24, 25). This simple realization removes the obstacle of having are more closely related to eukaryotes than are others, but it to culture all organisms in order to infer their characteristics, ignored the available molecular evidence as to which pro- and it permits all manner of new detailed characterizations of karyotes these were. This confusion was furthered by a drawing the populations in any given niche to be made. Perhaps the of the proposed relationships in which present-day organisms most dramatic demonstration of these new approaches to are not clearly distinguished from their ancestors.) microbial ecology is the discovery (through cloning and se- To date, over 1,500 prokaryotes have been characterized by quencing of genes directly from environmental samples) of two small-subunit rRNA sequencing. Figure 1 encapsulates pro- new groups of Archaea-both of which have to this point karyotic phylogeny as it is now known. Given the purview of defied cultivation (4, 10). One is a new family or order within this journal, our discussion will be limited to the two prokary- the euryarchaeotes, the other almost certainly a new taxon of otic domains. However, it is worthwhile to note in passing that even higher rank (see Pacific Ocean station 49 DNA clone molecular phylogeny has had an equally profound effect on our NH49-9, Santa Barbara Channel DNA clone SBAR5, and understanding of relationship among eukaryotes (eukaryotic Woods Hole DNA clone WHARQ in Fig. 1). For the first microorganisms in particular) and that anyone exposed to the time, it is possible to count not just flowers and beetles, but universal phylogenetic tree readily appreciates how artificial also microorganisms, in taking a census of life on this planet. the strong distinction between eukaryotes and prokaryotes has Another area in which evolutionary and comparative per- become. In Fig. 1, the split between the Archaea and Bacteria spectives have been invaluable has been the inference of is the primary phylogenetic division (in that the Eucarya have secondary and tertiary RNA structures. Comparisons of ho- branched from the same side of the tree as the Archaea [11, mologous RNA sequences from phylogenetically diverse or- 13]). ganisms have provided our current understandings of the Both prokaryotic domains would seem to be of thermophilic structures of rRNAs (9, 21, 22, 35), RNase P RNA (14), origin-suggesting that life arose in a very warm environment self-splicing introns (3, 20), signal recognition particle RNA (1, 2, 31). Among the Archaea, all of the Crenarchaeota (15, 18), and the small nuclear RNAs of the spliceosome (for cultured to date are thermophiles, and the deepest eur- a review, see reference 12). In several of these cases, it was yarchaeal branchings are represented exclusively by thermo- rRNA-based phylogenetic information that guided the choice philes. Among the Bacteria, the deepest known branchings are of organisms from which the corresponding molecules were again represented exclusively by thermophiles, and thermo- identified and sequenced. philia is widely scattered throughout the domain. Although our interests are primarily biological, to many The Archaea comprise a small number of quite disparate people the justification of any pursuit lies in its practical phenotypes that grow in unusual (to us, inhospitable) niches. consequences. The revolution in microbial ecology and the All are obligate or facultative anaerobes. As stated above, all inference of molecular structures do, of course, have direct (cultured) crenarchaeotes are thermophilic, some even grow- practical consequences (witness Applied and Environmental ing optimally above the normal boiling temperature of water. Microbiology and RNA-binding antibiotics), but it is the appli- The Archaeoglobales are sulfate reducers growing at high cation in clinical microbiology that most people would think of temperatures. The extreme halophiles grow only in highly first. Many clinically important microorganisms have now been saline environments (such as the Dead Sea and salt evapora- subjected to molecular phylogenetic analysis (e.g., 6, 26). tion ponds). The methanogens, which are responsible for These data and analyses have been used to develop molecular virtually all of the biologically produced methane on this diagnostics (e.g., 16) and to guide research into the nature (and planet, are confined to a variety of anaerobic niches, often control) of various pathogens. thermophilic. The universal phylogenetic tree brings us face to face with The Bacteria, on the other hand, are notable as being the the great evolutionary questions and allows us to formulate source of life's photosynthetic capacity. Five kingdoms of them in molecular terms.
FIG. 1. Prokaryotic phylogenetic tree of 253 representative species derived by maximum likelihood analysis of small-subunit rRNA sequences. The tree is abstracted from that provided by the Ribosomal Database Project (17), which is a composite of several trees inferred by using maximum likelihood (7, 23). The suggested rooting is that inferred for the universal tree (11, 13). Organisms are consecutively numbered and are indexed in the accompanying alphabetic listing (Table 1). Names of the major groups (31, 34) are indicated. The distance scale indicates the expected number of changes per sequence position, for those positions changing at the median rate...... I...... BCytophaga/Flexibacter/BacteroidesArchaeagroupc e i Aquifexpyrophilus Vesiculatum antarctica [158] h r oog ls [55] Flectobacillus glomeratus [159] Eurvarchaeota Methanosarcina barkeri [1] W | ~~~Flexibacter aggregans [1601 PetrotogaMethanosarcinamiothermathermophila[56] [2] Cytophaga uliginosa [161] 1 ~~~~~~~~~~GeotogaMethanosarcinapetraea [57]frisia [3] -Flavobacterium aquatile [162] 1 ~~~Fervidobacterium norJosum [581Methanococcoides methylutens [4] Cytophaga flevensis [163] I Thermosipho africanus [59] Methanohalophilus mahii [5] Fexibacter columnaris [164] I Termotoga maritima [60] Methanohalophilus oregonensis [6] lSporocytophaga cauliformis [165] breve Thermodesulfotobacterium commune [61] Methanolobus tindarius [7] [166] Methanohalobium evestigatum [8] - ~~~~~Weeksella virosa [167] 5 Methanohalophilus zhilinae [9] ~~~~FlavobacteriumMicroscilla aggregans subsp. catalatica~~~~~~~~~~~~~~~~~Green[168] Nonsulfur BacteriaI , MethanosaetaChloroflexusthermoacetophilaaurantiacus [62] [10] | yohaga fermentans [169] Herpetosiphon aurantiacus [63] Bacteroides distasonis [170] ThermomicrobiumMethanosaetaroseum 164]concilii [11] Methanoculleus marisnigri [12] ' ~~~~Bacteroides fragilis [171] Z thermophilus'Methanoculleus[65] thermophilicus [13]h a g~~~ytpag heparina [1721 DeinococusMethanoculleusradioduransbourgensis[66][14] Sphingobacterium mizutae [173] _ Methanogenium tationis, [15] ~~~~~~~~~~~~~~~~~~~~~~~Spirosomalinguale [174] |{ sancti C a o a tra&c lrpa t Methanospirillumrhungatei [16] ~~~~~~~Flexibacter [175] *~~~~~~~~Thermus Synechococcus sp. [67] Haliscomenobacter hydrossis [176] Methanocorpusculumhollandica [68] parvum [17] _ Methanogenium"cylindrica"organophilum[69] [18] Saprospira grandis [177] MethanomicrobiumMicroscillamobile [19]furvescens [178] _ sp. [70] , ~~~~~~~~Runellaslithyformis [1791 2 L ~~~DermocarpaMethanoplanussp. [71] limicola [20] Haloferax volcanii [21] ruber [1 80] __ ' ~~~~Prochloron didemni [72], ~~~~~~~~~~~~~~~~Flectobacillusmajor [181] ~~~~~ProchlorothrixOscillatoriaHalobacteriumsp. [73] halobium [22] _ Halococcus morrhuae [23] myxococcoides[182] ~~~~AnabaenaCyanophora paradoxa -- cyanelle [74] hutchinsonii [183] _ Halobacterium~~~~~~~~~~Chlamydomonasmarismortuireinhardii[24]--chloroplast [75] _ ~~~~~Nostoc Thermoplasma~~~~~~~~~~Chlorobium-- acidophilumvibrioforme[25] ' Zea chloroplast [76][184] ma~~~~ys Channel bacterioplankton DNA clone SBAR16 [26] _ caldariumSanta--Barbarachloroplast [77] ~~~~~Cyanidium ~~~~~~~FlexibacterWoods Hole bacterioplankton DNA clone WHARN [27] Fibrobvacteria IIl | r - ~~~~~~~~~~~~~~~~~~~~~~Euglenagracilis --chloroplast [78] Archaeoglobus fulgidus [28], ,Fibrobacterdanicaintestinalis [185] chloroplast [79] Methanothermus fervidusGloeobacter[29] "violaceus"~~~~~~~~~~~~~~~~Sporocytophaga[80] 'Fibrobacter succinogenes [186] |n Methanobacterium thermoautotrophicum [30] ~~~~Cytophaga l Methanobrevibacter arboriphilus-t--~~~~~~~~~~~~~[31] G+C Gram-Positive~SpirochaetesBacteria Methanosphaera stadtmanii Leptonema[32] illini [187] Leuconostoc mesenteroides subsp. mesenteroides [81] Methanobacteriumeptos~Letopiraformicicum [33] interrogans serovar pomona [188] Leuconostoc oenos [82] Methanobacterium, bryantii [34] ~~~~~~~~~Treponema sp. [189] I Lactobacillus viridescens [83) Methanococcus jannaschii [35] _ ~~~~~~~~~~Serpulahyodysenteriaeparamesenteroides[190] [84], Methanococcus igneus_[36]_ ~~~~~~~Ochromonas_ Lactobacillus~~~~~~~~~~~Treponemaamylophiluspallidum[85][191] Methanococcus thermolithotrophicus [37] . l Spirochaeta~ stenostrepta~~~Lactobacillus[192]delbrueckii [86] l "Methanococcus| aeolicus" [38] L Treponema saccharophilum [193] Lactobacillus acidophilus [87] Methanococcus maripaludis [39] _- PediococcusSpirochaetapentosaceuslitoralis [88][194] Methanococcus~~~~~~~~~~~~~Lowvannielii [40]_Lactobacillus brevis [89] burgdorferi [195] _ Methanococcus voltae [41] Lactobacillus ruminis [90][196] Thermococcus celer [42] FlexistipesrL sinusarabiciL~~~actobacillus[197]casei subsp. casei [91] Methanopvrus kandleri [43] I Carnobacterium piscicola [921 i ||| H Enterococcus faecalis [93] ~~~~~~~~~~Planctomyces/Chlamydia^en - Ln-e-group- , ~~~~~~~~~~Chlamydia~~~~Leuconostocpsittaci [198]salivarius L;renarcnaeoia L [94] WoodsrHole bacterioplanktonLactococcusDNA~~~~~~~PlanctomycesclonelactisWHARQsubsp.staleyilactis[44] [199][95] 4{C-ListeriaSantamonocytogenesBarbara Channel[96] bacterioplankton DNA clone SBAR5 [45] | ~~~~KurthiaPacific^W^^..,W>W.Y.ffIsosphaerOceanzopfii [97]station 49 bacterioplankton DNA clone NH49-9pallida*[200[46] Sulfolobus shibataeX | [47]' ~~~Bacillus subtilis [981 Purple Bacteria (Proteobacteria Sulfolobus solfataricus [48] Gemella haemolysans[99] Pyrodictium occultum [49] Spirochaeta~~~~~~~~~~Borrelia anaerobium [100]Delta & Epsilon subdivisionI Closridum [01]Asteroleplasma - Desulfurococcus mobilis,Desulf[50] uromonas~~~~~~~~~~~~~aurantiaacetoxidans [201] - Thermofilum pendens [51] _ ~~~~~~Desulfosarcina variabilisClostridium[202] innocuum [102] Thermoproteus tenax [52] Bdellovibrio stolpii [203]Eubacterium biforme [103] QPyrobaculum islandicum| [53] Nannocystisexedensrhusiopathiae[204] [104] 4|Pyrobaculum_l .aerophilum|[54] aurantiaca [205] infecting Oenothera hookeri [105] i I ^ ' ~~~~~~Myxococcus xanthus [206] Acholeplasma laidlawii [106] ~~~~~~~~~~~~~~~~~~~~StreptococcusDesulfovibrio desulfuricans [207] | ~~~~Anaeroplasma bactoclasticum [1107] ThiovulumMycoplasmasp. [208]ellychnium [108] CampylobacterMycoplasmajejuni [209]capricolum [109] ,Wolinella| ' succinogenes~~Spiroplasma[210]apis[110] Helicobacter pylori [211] rl L ~~~~Spiroplasma citri [1 1 1] Spiroplasmasp. [1112] | Mycoplasma hyopneumoniae~~~~~~~~~~~~~~~Alpha[113] subdivision | Methylobacterium extorquens [212]sualvi [1 14] Beijerinckia indicaMycoplasma[213] hominis [115] Hyphomicrobium vulgare [214] Ureaplasmaurealyticum[116] | -Rhodomicrobium vannielii [215] gallisepticum [1117] .| Agrobacterium tumefaciens [216] Mycoplasma pneumoniae [1 18] | Brucella abortus [217] |~~~~~~~~ErysipelothrixClostridium| thermoaceticum [119] 5-~~~~~~~Syntrophospora~~~~~Stigmatella~~~~~~~~~~~~~MLORochalimaeabryantii [120]quintana [218] | =1 I ~~~~~~~~~Rhodopseudomonas marina subsp. agilis [219] I2 . I l ~~~~~~~~Clostridium sporosphaeroides [1121] mitochondrion |
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