Evolutionary ecology during the rise of dioxygen in the Earth's atmosphere

Abstract

Pre-photosynthetic niches were meagre with a productivity of much less than 10 K4 of modern photosynthesis. Serpentinization, arc volcanism and ridge-axis volcanism reliably provided H 2 . Methanogens and acetogens reacted CO 2 with H 2 to obtain energy and make organic matter. These skills pre-adapted a bacterium for anoxygenic photosynthesis, probably starting with H 2 in lieu of an oxygen 'acceptor'. Use of ferrous iron and sulphide followed as abundant oxygen acceptors, allowing productivity to approach modern levels. The 'photobacterium' proliferated rooting much of the bacterial tree. Land photosynthetic microbes faced a dearth of oxygen acceptors and nutrients. A consortium of photosynthetic and soil bacteria aided weathering and access to ferrous iron. Biologically enhanced weathering led to the formation of shales and, ultimately, to granitic rocks. Already oxidized iron-poor sedimentary rocks and low-iron granites provided scant oxygen acceptors, as did freshwater in their drainages. Cyanobacteria evolved dioxygen production that relieved them of these vicissitudes. They did not immediately dominate the planet. Eventually, anoxygenic and oxygenic photosynthesis oxidized much of the Earth's crust and supplied sulphate to the ocean. Anoxygenic photosynthesis remained important until there was enough O 2 in downwelling seawater to quantitatively oxidize massive sulphides at mid-ocean ridge axes.

How oxygen reacts with oxygen-tolerant respiratory [NiFe]-hydrogenases

“…Nickel, an element not normally associated with enzymatic O 2 activation, was available to biology much earlier in Earth's history than copper (40,41); in fact [NiFe]-hydrogenases are considered to be among the most ancient enzymes (42). Hydrogen sourced from geological processes (e.g., hydrothermal circulation through basalt and serpentinite, arc volcanism, and ridge-axis volcanism) was available for metabolism long before atmospheric levels of O 2 began to rise (41). A slow rise in O 2 concentrations would have driven hydrogenase evolution, first to merely survive (transient) O 2 exposure, and later to develop true O 2 tolerance to sustain H 2 oxidation in a microaerobic respiratory chain with newly evolved full-fledged terminal, iron-containing cytochrome bd oxidases.…”

Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments

“…Since the onset of global oxygenation of the shallow ocean and the atmosphere about 2.4 billion yr ago (Sleep & Bird 2008), there have been times when the euxinic and sulfidic conditions in the ocean have included parts of the euphotic zone, much as in the present-day Black Sea and some Antarctic fjords. There is biomarker evidence for the occurrence of sulfide-oxidising anoxygenic Bacteria of the Chlorobi and the Chromatiaceae in the marine photic zone in the mid-Proterozoic oceanic some 1.64 billion yr ago (Brocks et al 2005).…”

The Hadean-Archaean Environment

“…It is far more oxidized than mantle-derived igneous rocks (Lecuyer and Ricard 1999). The excess oxygen exceeds that to balance buried reservoirs of organic carbon (see Sleep and Bird 2008). It is likely that biological methane from photosynthesis allowed H 2 to escape to space before the oxidation of the Earth's atmosphere at $2.45 Ga (Catling et al 2001), leaving the oxygen from water behind.…”

“…Battistuzzi et al (2004) and Battistuzzi and Hedges (2009) proposed that most bacteria clades descend from the original photosynthetic ancestor. Sleep and Bird (2008) called the clade descending from the original photosynthesizer with the obvious informal name Photobacteria. Battistuzzi et al (2004) and Battistuzzi and Hedges (2009) further divided Photobacteria into Hydrobacteria that remained in the ocean and Terrabacteria that colonized land.…”

“…With regard to the rock record, Sleep and Bird (2008) noted that the photosynthetic Terrabacteria colonists faced a dearth of FeO and sulfide on land. Sulfur (0.1% in basalt [e.g., and Bird 1995]) is much less common than FeO ($10% in basalt [e.g., Krauskopf and Bird 1995]) in most common rocks.…”