Hydrothermal vents and the origin of life
William Martin
University of Düsseldorf, Germany
Abstract
Darwin was not primarily concerned with microbes, and it is arguably true that the most incisive insights that we have obtained into the evolutionary process since the New Sysnthesis have concerned the evolution of microbes. As recently as 10 years ago, it was widely held that some eukaryotes primitively lacked mitochondria and were true intermediates in the prokaryote-to-eukaryote transition. That idea focussed much research on anaerobic and parasitic eukaryotes, which turned out to have mitochondria that were either previously overlooked or not recognized as such. Today, mitochondria, including their manifestations among anaerobic forms — hydrogenosomes and mitosomes —, are known to be ubiquitous among eukaryotes, at odds with older theories that held eukaryotes to be direct descendants of a prokaryote via direct filiation, but consistent with the predictions of theories that apporach the origin of mitochondria from the standpoint of a symbiosis between prokaryotes. This view has it that eukaryotes thus arose from prokaryotes, hence the origin of life boils down to the origin of prokaryotes, among which two main groups — the archaebacteria and the eubacteria — are recognized. And whence did prokaryotes arise? Submarine hydrothermal vents are geochemically reactive habitats that harbour rich microbial communities. There are striking parallels between the chemistry of the H2–CO2 redox couple that is present in hydrothermal systems and the core energy metabolic reactions of some modern prokaryotic autotrophs. The biochemistry of these autotrophs might, in turn, harbour clues about the kinds of reactions that initiated the chemistry of life. Hydrothermal vents are now a point where microbiology and geology meet, thereby breathing new life into research into one of biology’s most important questions — the origin of life.
Selected references:
Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393:162–165.
Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41.
Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99: 12246–12251.
Martin W, Russell MJ (2003) On the origins of cells: An hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil. Trans Roy. Soc. Lond. B 358:59–85.
Timmis JN, Ayliffe MA, Huang CY, Martin W(2004) Endosymbiotic gene transfer: Organelle genomes forge eukaryotic chromosomes. Nature Rev. Genet. 5:123–135.
Martin W, Koonin EV(2006) Introns and the origin of nucleus-cytosol compartmentation. Nature 440:41–45.
Embley TM, Martin W (2006) Eukaryote evolution: changes and challenges. Nature 440:623–630.
Dagan T, Martin W (2007) Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution. Proc. Natl. Acad. Sci. USA 104:870–875.
Martin W, Russell MJ (2007) On the origin of biochemistry at an alkaline hydrothermal vent. Phil. Trans Roy. Soc. Lond. B 367:1887–1925.
Dagan T, Artzy-Randrup Y, Martin W (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc. Natl. Acad. Sci. USA 105:10039–10044.
Martin W, Baross J, Kelley D, Russell MJ (2008) Hydrothermal vents and the origin of life. Nature Rev. Microbiol. 6:805–814.