Cell evolution and Earth history: stasis and revolution

Abstract

This synthesis has three main parts. The first discusses the overall tree of life and nature of the last common ancestor (cenancestor). I emphasize key steps in cellular evolution important for ordering and timing the major evolutionary innovations in the history of the biosphere, explaining especially the origins of the eukaryote cell and of bacterial flagella and cell envelope novelties. Second, I map the tree onto the fossil record and discuss dates of key events and their biogeochemical impact. Finally, I present a broad synthesis, discussing evidence for a three-phase history of life. The first phase began perhaps ca 3.5 Gyr ago, when the origin of cells and anoxic photosynthesis generated the arguably most primitive prokaryote phylum, Chlorobacteria (ZChloroflexi), the first negibacteria with cells bounded by two acyl ester phospholipid membranes. After this 'chlorobacterial age' of benthic anaerobic evolution protected from UV radiation by mineral grains, two momentous quantum evolutionary episodes of cellular innovation and microbial radiation dramatically transformed the Earth's surface: the glycobacterial revolution initiated an oxygenic 'age of cyanobacteria' and, as the ozone layer grew, the rise of plankton; immensely later, probably as recently as ca 0.9 Gyr ago, the neomuran revolution ushered in the 'age of eukaryotes', Archaebacteria (arguably the youngest bacterial phylum), and morphological complexity. Diversification of glycobacteria ca 2.8 Gyr ago, predominantly inhabiting stratified benthic mats, I suggest caused serial depletion of 13 C by ribulose 1,5-bis-phosphate caboxylase/oxygenase (Rubisco) to yield ultralight late Archaean organic carbon formerly attributed to methanogenesis plus methanotrophy. The late origin of archaebacterial methanogenesis ca 720 Myr ago perhaps triggered snowball Earth episodes by slight global warming increasing weathering and reducing CO 2 levels, to yield runaway cooling; the origin of anaerobic methane oxidation ca 570 Myr ago reduced methane flux at source, stabilizing Phanerozoic climates. I argue that the major cellular innovations exhibit a pattern of quantum evolution followed by very rapid radiation and then substantial stasis, as described by Simpson. They yielded organisms that are a mosaic of extremely conservative and radically novel features, as characterized by De Beer's phrase 'mosaic evolution'. Evolution is not evenly paced and there are no real molecular clocks.

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

“…so far failed to provide strong support for any of the hypotheses for eukaryogenesis in common currency (Rivera & Lake 2004;Cavalier-Smith 2006).…”

“…The origins of eukaryotic [Fe]-hydrogenase and PFO are also part of a bigger question concerning the origins of the eubacterial-like genes that encode much of eukaryote metabolism (Ribeiro & Golding 1998;Rivera et al 1998;Esser et al 2004). There are a number of imaginative hypotheses to explain these genes; as the product of multiple lateral transfers from different prokaryotes (Doolittle 1998), or the legacy of different eubacteria that participated in eukaryogenesis (Martin & Mü ller 1998;Moreira & LopezGarcia 1998;Rivera & Lake 2004;Cavalier-Smith 2006). Genomics coupled with more sophisticated phylogenetic analyses, should in principle be able to resolve gene origins, or at least reveal the limits of resolution that the data can provide (Penny et al 2001;Ho & Jermiin 2004;Roger & Hug 2006).…”

“…It thus seems possible that all eukaryotes might contain an organelle of mitochondrial ancestry, emphasizing the pivotal role that the mitochondrial endosymbiosis has played in eukaryotic evolution. Although we still need a reliable root for the eukaryotic tree (see Cavalier-Smith 2006;Roger & Hug 2006), it is evident that anaerobic eukaryotes have repeatedly arisen from within ancestrally aerobic groups with mitochondria. Anaerobic eukaryotes are neither rare nor primitive as once thought.…”

Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia

“…Relative node ages were estimated using R8S 1.7 (Sanderson 2002) by rate-smoothing the ML tree using penalized likelihood and a log-smoothing parameter of 5, selected as optimal by cross-validation (Sanderson 2003). Absolute ages were estimated by setting the minimum and maximum age of the Chlorophyta-Streptophyta split at 700 and 1500 Ma, based on the fossil record and molecular clock estimates (Douzery et al 2004;Hedges et al 2004;Yoon et al 2004;Berney & Pawlowski 2006;Cavalier-Smith 2006;Roger & Hug 2006;Zimmer et al 2007;Herron et al 2009). …”

Light and the evolution of vision

“…Such eukaryotes originated probably between 800 and 1200 million years ago, 17 but prokaryotes have been present in the fossil record around 1500 million years earlier. 18 Lynn Margulis presented the theory by which eukaryotes form through endophagy of prokaryote algae to produce chloroplasts and bacteria to yield mitochondria, both examples of endosymbiosis. 19 So we should look for the origin of these eukaryote photopigments in prokaryote bacteria.…”