Energetics and genetics across the prokaryote ... - Biology Direct

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Lane Biology Direct 2011, 6:35http://www.biology-direct.com/content/6/1/35Page 2 of 31hard to distinguish between eukaryotic and prokaryoticmicrofossils let alone prove the existence of extinct linesof protoeukaryotes. While asserting the unprovable existenceof extinct lines of eukaryotes is unsatisfying, if notunscientific, extinction is commonplace, and the argumentseems, on the face of it, irrefutable.But there are several reasons to doubt that prokaryoteshave repeatedly given rise to more complex ‘protoeukaryotes’,which were ultimately all driven to extinction bymodern eukaryotes that came to occupy every niche. Theperiodic mass extinctions of plants and animals, followedby evolutionary radiations of hitherto suppressed groups,are not characteristic of microbial evolution-such radiationsexplore morphological, not metabolic, space. Moreover,large animals and plants generally have tinypopulations in comparison with microbes, and cannotacquire life-saving genes by lateral gene transfer, makinganimals and plants much more vulnerable to extinction.The continuity of global geochemical cycles over threebillion years [4] shows that no major prokaryotic grouphas been driven to extinction, not even methanogens andacetogens, the most energetically tenuous forms of life.The abundance of apparently parallel niches [5] suggeststhat extinction is not the rule. Archaea, once believed tobe restricted to extreme environments such as hydrothermalvents and salt flats, are common in temperate oceans[6], whereas eukaryotes, long thought to be excludedfrom extreme environments by their delicate constitutions,are in fact abundant in anoxic conditions [7] and inrivers contaminated with heavy metals [8]. Picoeukaryotescompete directly with prokaryotes in many environments[9], yet neither group has fallen extinct.Extinction seems too facile an explanation to accountfor fact that all complex life on Earth shares a commonancestor that only arose once. If indeed many other independentlyarising lineages of protoeukaryotes all fellextinct, more persuasive reasons are needed than simpledisplacement by more competitive modern eukaryotes.The existence of a diverse group of morphologicallysimple eukaryotes that occupy an intermediate nichebetween prokaryotes and more complex protists refinesthis point. Described as archezoabyCavalier-Smithinthe 1980s [10,11], the group was seen as primitively amitochondriateprotoeukaryotes, living fossils of the prokaryotic-eukaryotictransition [12,13]. Genetic andmorphological studies, however, revealed that all knownarchezoa possessed mitochondria in the past, and lostthem via reductive evolution to specialised organellescalled hydrogenosomes and mitosomes [14-17]. This issignificant in terms of extinction. There are at least 1000species of simple protist that lack mitochondria, yet all ofthem evolved by reductive evolution from more complexancestors, rather than evolving ‘up’ from more simpleprokaryotes. Considered purely in terms of chance, thelikelihood of this is around one in 10 300 against. Allowingfor independent phylogenetic origins on a more realistic20 separate occasions, the probability is still one in amillion. This pattern is unlikely to be chance. Eitherthere was a competitive advantage to reductive evolution(but if so, why should complex aerobic protists displaceanaerobic specialists by becoming more like them?) orthere was heavy selection against prokaryotes evolvinggreater morphological complexity. That seems to be true.Prokaryotes show no tendency to evolve greatermorphological complexityDespite their metabolic virtuosity, living prokaryotes arebarely distinguishable from 3-billion year old microfossilsin their morphological appearance [18]. At a molecularlevel there is no obvious reason for this limitation: bacteriamadeastartupeveryavenueofcomplexity,butthen stopped short. There are prokaryotic examples ofstraight chromosomes [19], DNA recombination [20],multiple replicons [21], introns and exons [22], extremepolyploidy [23], nucleus-like structures [24], internalmembranes [25], giant size [26], dynamic cytoskeleton[27], predation [28], parasitism [29], intercellular signalling[30], endocytosis [31], even endosymbionts [32,33].What prokaryotes lack is the characteristic eukaryoticaccumulation of all of these traits at once, typically inmuch larger cells with complex internal compartmentsand intracellular transport networks, all encoded by genomesthat range freely from bacterial size up to scores ofGigabases, even in protists [34]. The absence of real morphologicalcomplexity in bacteria is plausibly ascribed tothe dominant mode of prokaryotic evolution: prokaryotesare streamlined by selection for small genomes and fastreplication, quickly losing unnecessary genes, and frequentlyacquiring new genes from the metagenome,when needed, by lateral gene transfer [35,36].But why are eukaryotes not equally subject to heavyselection for streamlining? Some are, certainly, but manyare not, and most eukaryotic streamlining appears to besecondary. Population geneticists ascribe the accumulationof genes in eukaryotes to reduced purifying selectionin small populations [37]; but if so, why don’t smallerpopulations of prokaryotes accumulate larger genomesfor exactly the same reasons? If the constraint was circularchromosomes [38] why didn’t bacteria with straightchromosomes and multiple replicons become complex?If phagocytosis was the critical step [39,40], what stoppedwall-less prokaryotes with an incipient capacity for endocytosis(protein uptake) and dynamic cytoskeletons fromevolving true complexity? This is ultimately a questionabout the nature of natural selection. If traits such as thenucleus, phagocytosis and meiotic sex evolved by naturalselection acting on ordinary mutations in large or smallpopulations of prokaryotes, and each step offered an
Lane Biology Direct 2011, 6:35http://www.biology-direct.com/content/6/1/35Page 3 of 31advantage, then why did the same traits not evolverepeatedly in prokaryotes, as did the eye [41] in eukaryotes?As noted already, there is no reason to supposethat such protoeukaryotes should have been driven toextinction by more competitive modern eukaryotes;rather, prokaryotes just seem to have no proclivity toexplore morphological space.Eukaryotes originated in an endosymbiosis betweenprokaryotesThe fact that all eukaryotic cells either have, or oncehad, mitochondria, means that the acquisition of mitochondriaby some host cell was at the very least an earlyevent in eukaryotic evolution. And large scale, genomewidephylogenetic studies [42-46] suggest that an endosymbiosisbetween prokaryotes might well have been thesingular event that broke the eternal loop of prokaryoticsimplicity.There is little doubt that the ancestor of the mitochondriawas a free-living bacterium, probably most closelyrelated to a-proteobacteria [47] (whatever they were 1.5-2billion years ago), but its metabolic capabilities are uncertainand disputed [48]. However, given the ubiquitous phylogeneticdistribution of anaerobic mitochondria andhydrogenosomes across all the eukaryotic supergroups[49], the most parsimonious answer is that the mitochondrialancestor was a metabolically versatile, facultativelyanaerobic bacterium, perhaps similar to Rhodobacter [50].The identity of the host cell is even more contentious[51,52]. Most large-scale genomic analyses point to abona fide prokaryote, an archaeon of some sort [42-46],albeit not falling clearly into any modern group, soagain its metabolic capabilities are unknown. It is thereforedifficult to reconstruct the relationship between theendosymbiont and host cell by phylogenetics alone. Acommon argument against this scenario (an endosymbiosisbetween two prokaryotes) is that one prokaryotecould not have gained entry to another except throughphagocytosis. This argument is refuted by two knownexamples of prokaryotic cells living within other prokaryotes[32,33] (Figure 1)–plainly it is possible, even ifextremely uncommon. Indeed, the very improbability ofsuch an event helps to explain the unique origin ofeukaryotes [53]. (It should also be noted that endosymbiontsare also known in fungi, despite the fact thatfungi are no more phagocytic than bacteria [54].)Because phylogenetics cannot presently constrain theidentity of either host cell or endosymbiont, it cannotgive a clear insight into eukaryogenesis–the crossing ofthat deep gulf between prokaryotes and eukaryotes. Onecell inside another cell may have broken the eternalprokaryotic loop, but this situation is far removed fromthe morphological complexity of even the simplesteukaryotic cell. Is it possible to gain an insight intowhat happened next without the aid of phylogeneticreconstruction?Cell fusions best explain the accumulation ofeukaryotic traitsAny hypothesis for the origin and evolution of eukaryotesmust explain why prokaryotes showlittletendencytoevolve morphological complexity; why the Last EukaryoticCommon Ancestor, LECA, was morphologically complex;and why no true evolutionary intermediates exist,despite the niche being viable, and indeed filled withthousands of simple protists [10,11]. Prokaryotes andeukaryotes both speciate profligately, meaning thatgenetic variation falls into innumerable discrete clusters,which correspond to species as defined by Darwin andelaborated by Mallet [55]. Despite this universal tendencyto vary and diverge, there was no successful speciationacross the prokaryote-eukaryote transition. That is to say,there are no surviving evolutionary intermediates–no‘early branching’ species, equivalent to the discreditedarchezoa, despite the great evolutionary distance crossed.If the arguments marshalled here are correct, the trigger,or starting point, for eukaryogenesis was an endosymbiosisbetween prokaryotes: a prokaryote within a prokaryote,lacking a nucleus or any of the other signatureeukaryotic traits. In contrast, LECA was recognizablyeukaryotic, with a nucleus, straight chromosomes, intronsand exons, a cell cycle, meiosis and mitosis, dynamiccytoskeleton, motor proteins and intracellular transportmechanisms, endomembrane systems and mitochondria.All of these traits apparently evolved in a population ofcells that never diverged to form a successful earlybranchingspecies. There are no evolutionary intermediateswith a nucleus but no endoplasmic reticulum, ormitochondria but no nucleus, or a dynamic cytoskeletonbut no meiosis. Over this long evolutionary distance, theprokaryote-eukaryote transition, the tree of life is neithera branching tree nor a reticular network, but whatamounts to an unbranching trunk (Figure 2).Only certain forms of inheritance could begin toexplain such a trunk. Being inherently asymmetric, lateralgene transfer surely cannot explain the universalityof eukaryotic basal traits: it is far more likely to give riseto the pattern that is actually seen in prokaryotes, inwhich different species possess different traits, and nonepossesses them all. But reciprocal sex (or some form ofcell fusion) can readily explain the accumulation ofeukaryotic traits. If so, then sex must have arisen veryearly in eukaryotic evolution, as is borne out by phylogeneticanalyses [56-58]; but here this is a logical inference,not an observation.Likewise, the evolution of eukaryotes must have beenrapid, in a small population. If the population had beenlarge, the individual cells should have been successful
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