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Early Microbial Evolution: the Age of Anaerobes

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Early Microbial Evolution: the Age of Anaerobes Downloaded from http://cshperspectives.cshlp.org/ on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press Early Microbial Evolution: The Age of Anaerobes William F. Martin and Filipa L. Sousa Institute for Molecular Evolution, University of Du¨sseldorf, 40225 Du¨sseldorf, Germany Correspondence: [email protected] In this article, the term “early microbial evolution” refers to the phase of biological history from the emergence of life to the diversification of the first microbial lineages. In the modern era (since we knew about archaea), three debates have emerged on the subject that deserve discussion: (1) thermophilic origins versus mesophilic origins, (2) autotrophic origins versus heterotrophic origins, and (3) how do eukaryotes figure into early evolution. Here, we revisit those debates from the standpoint of newer data. We also consider the perhaps more pressing issue that molecular phylogenies need to recover anaerobic lineages at the base of prokary- otic trees, because O2 is a product of biological evolution; hence, the first microbes had to be anaerobes. If molecular phylogenies do not recover anaerobes basal, something is wrong. Among the anaerobes, hydrogen-dependent autotrophs—acetogens and methanogens— look like good candidates for the ancestral state of physiology in the bacteria and archaea, respectively. New trees tend to indicate that eukaryote cytosolic ribosomes branch within their archaeal homologs, not as sisters to them and, furthermore tend to root archaea within the methanogens. These are major changes in the tree of life, and open up new avenues of thought. Geochemical methane synthesis occurs as a spontaneous, abiotic exergonic reac- tion at hydrothermal vents. The overall similarity between that reaction and biological meth- anogenesis fits well with the concept of a methanogenic root for archaea and an autotrophic origin of microbial physiology. riting about early microbial evolution is a given that FeS clusters are basically minerals, Wdaunting task, so it was possibly unwise hence ancient, and that oxygen comes from cy- to agree to do it. At present, there is a lot going anobacteria, cyanobacteria in turn being too on—news to report and new things to think complex in physiology to be the most ancient about. Some of the current news has to do prokaryotes. In that view, life got off to an an- with phylogenetic trees. Trees tend to change aerobic start, with help from minerals, with ox- over time as new data and methods emerge. ygen being a biological invention that microbes Before there were trees (molecular phylogenies), gradually learned to live with. That is a reason- the study of microbial evolution was about put- able proposition. ting chemical processes in sequence. Eck and Before it was known that methanogens are Dayhoff (1966), for example, had iron–sulfur archaea, Decker et al. (1970) ordered the emer- (FeS) proteins like ferredoxin and strict anaer- gence of physiological phenotypes along a obes like clostridia early, a reasonable premise sequence from strict anaerobes via facultative Editor: Howard Ochman Additional Perspectives on Microbial Evolution available at www.cshperspectives.org Copyright # 2016 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a018127 Cite this article as Cold Spring Harb Perspect Biol 2016;8:a018127 1 Downloaded from http://cshperspectives.cshlp.org/ on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press W.F. Martin and F.L. Sousa anaerobes to aerobes and from autotrophs and the early historyof life. That was the plan at least, fermenters to phototrophs and heterotrophs. and it would definitely work, as long as lateral Their scheme had clostridia and methanogens gene transfer (LGT), which genomes uncovered (having cobalamin) branching first, followed by as a powerful mechanism in prokaryote genome sulfate reducers (having heme), then by bacte- evolution (Ochman et al. 2000), had not scram- rial photosynthesizers (having chlorophylls) bled history too much (Dickerson 1980). The and diverse bacteria having respiratory chains, issue of how tree-like prokaryote evolution is including forms that use oxygen as a terminal or is not (because of LGT) is still simmering. acceptor. That is also a reasonable proposition. Some say that prokaryote evolution is tree-like (For illustration, we have based our scheme in (Ciccarelli et al. 2006; Boussau and Gouy 2012), Fig. 1 and Fig. 2 on data in Figure 11 in Decker some say that it is somewhat tree-like (Puigbo` et al. 1970.) et al. 2009), some say that “only 1%” is tree-like The rRNA revolution and the discovery of (Dagan and Martin 2006), some say that we can- archaea changed everything, of course (Woese not tell, so we should assume that it is tree-like and Fox, 1977; Woese 1987), and the evolution (Forterre 2015), while some say “can we just get of prokaryotes became something one could on with it” (Lawrence and Hendrickson 2003). investigate using trees. With ribosomal RNA se- Microbiologists always knew about LGT, quences, one could suddenly do trees, as accu- having even built a tolerance of up to 30% dif- rately as desired or as accurately as possible, sort ference in gene content between strains of the out the branches, plot characters across those same species into the species definition (Wayne branches—just like in vertebrate phylogeny— et al. 1987; Stackebrandt and Ebers 2006), there- and infer ancestral states so as to possibly read by fully anticipating the exciting findings from Anaerobes Aerobes Aerotolerant Obligate Facultative Obligate obligate Clostridia, Sulfate- Purple and green Lactobacilli and Enterobacteria, Pseudomonas, methane-forming reducing sulfur bacteria propionibacteria Athiorhodaceae Corynebacteria bacteria bacteria – Cytochrome oxidases + Oxygenases + Phorbin + Cytochrome oxidases + Porphin + Corrin Redrawn from Primordial anaerobes Decker et al. 1970 Figure 1. Biological steps in the evolution of microbial metabolism as posited 45 years ago. (Based on Figure 11 in Decker et al. 1970.) 2 Cite this article as Cold Spring Harb Perspect Biol 2016;8:a018127 Downloaded from http://cshperspectives.cshlp.org/ on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press Early Microbial Evolution H2O H2O O2 Aerobic respiration Oxygenic Haloarchaea photosynthesis Anaerobic photosynthesis Other archaea Chlorophyll Cytochromes Anaerobic and respiration quinones Fermentations Fermentations Cytochromes and quinones Na+ Acetyl-CoA CH3-CoFeSP CH4 ADP + Pi CO ATP CoM-S-S-CoB Acetyl-P ADP ADP + Pi ATP HS-CoB 2 H2 + Pi CO2 CH3-THF CH -S-CoM 3 Fdox ATP NAD+ MtrA-H Acetate NADH 2– CH -H MPT Fd CH2-THF 3 4 NAD+ Na+ F Eha/ 420 Ehb H 2 H2 NADH 2 F420H2 H CH-THF CH -H MPT 2 2 4 2 Na+ Fdox F420 CH -CoFeSP Rnf H 3 2 F420H2 2– 2– + CO Fd Fd CHO-THF CH-H4MPT 2 Na+ ADP + Pi ATP CO NADH Formate CHO-MFR Acetyl-CoA 2 + 2 H Fdox Fd2– H2 CO2 CO2 Biosynthesis Bacteria Archaea (acetogens) (methanogens) Corrins LUCA (last universal common ancestor) Hydrothermal setting Figure 2. A possible sequence of events in early evolution starting from alkaline hydrothermal vents. (Legend continues on following page.) Cite this article as Cold Spring Harb Perspect Biol 2016;8:a018127 3 Downloaded from http://cshperspectives.cshlp.org/ on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press W.F. Martin and F.L. Sousa genomics that prokaryotes have pangenomes humans have no alternative but to report sub- (Lapierre and Gogarten 2009; Koonin 2010). jectively, based on their scientific background, With such a turbulent background for the study what they have learned and what they believe to of early evolution, hot debates were sure to fol- be true (what premises they embrace). That is low, most of which will never be resolved to particularly true for early evolution, because the everyone’s satisfaction, because there are so topic is so broad, and many of its central prob- many unknowns about early microbial evolu- lems underdetermined. Articles in Wikipedia tion, which makes it so interesting. are not signed by their authors, so we cannot Before going any further, a caveat is in order. see who wrote them; hence, we cannot begin The study of early evolution will always be a to wonder what schools and biases are behind controversial topic because it is so far removed the reporting. Scientific papers have author from today in time that we will never know names on them, making the nature of the (in- exactly (or perhaps even approximately) what nate) subjectivity more transparent. Truly ob- happened. But, scientists and the taxpayers jective reporting on early evolution is not pos- who fund science nonetheless generally want sible: the ideas are diverse, the literature is vast, to know something about early evolution and nobody knows all of it, and one cannot write have well-justified expectations that specialists about all of the ideas in one essay. The reader is (like us) should be able to report on the topic thus warned that we will be reporting from our in a readable form. It is perhaps unfortunate, particular viewpoint and that some microbiol- though, that many taxpayers and many scien- ogists generally agree with what we are saying tists will never turn to the scientific literature for here, while others do not, which is fine. information about early evolution, consulting For the purpose of this article, the term Wikipedia or some other web-based informa- “early microbial evolution” designates the phase tion storage and retrieval system instead. Why is of evolution from the emergence of life to the that unfortunate? Because Wikipedia, despite its divergence of the first microbial lineages. In the aura of objectivity, is written by humans and modern era (since we knew about archaea), Figure 2. (Continued) Simplified scheme of energy metabolism showing the similarities between acetate (left) and methane (right) formation from H2 and CO2 by acetogenic bacteriawithout cytochromes (the map shown is for Acetobacterium woodii, based on data in Schuchmann and Mu¨ller 2014) and hydrogenotrophic methano- genic archaea (from data in Buckel and Thauer 2013).
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