Origin and early evolution of photosynthetic eukaryotes in freshwater environments: reinterpreting proterozoic paleobiology and biogeochemical processes in light of trait evolution

Abstract

Phylogenetic analyses were performed on concatenated data sets of 31 genes and 11,789 unambiguously alignable characters from 37 cyanobacterial and 35 chloroplast genomes. The plastid lineage emerged somewhat early in the cyanobacterial tree, at a time when Cyanobacteria were likely unicellular and restricted to freshwater ecosystems. Using relaxed molecular clocks and 22 age constraints spanning cyanobacterial and eukaryote nodes, the common ancestor to the photosynthetic eukaryotes was predicted to have also inhabited freshwater environments around the time that oxygen appeared in the atmosphere (2.0-2.3 Ga). Early diversifications within each of the three major plastid clades were also inferred to have occurred in freshwater environments, through the late Paleoproterozoic and into the middle Mesoproterozoic. The colonization of marine environments by photosynthetic eukaryotes may not have occurred until after the middle Mesoproterozoic (1.2-1.5 Ga). The evolutionary hypotheses proposed here predict that early photosynthetic eukaryotes may have never experienced the widespread anoxia or euxinia suggested to have characterized marine environments in the Paleoproterozoic to early Mesoproterozoic. It also proposes that earliest acritarchs (1.5-1.7 Ga) may have been produced by freshwater taxa. This study highlights how the early evolution of habitat preference in photosynthetic eukaryotes, along with Cyanobacteria, could have contributed to changing biogeochemical conditions on the early Earth.

Contrasting microfossil preservation and lake chemistries within the 1200–1000 Ma Torridonian Supergroup of NW Scotland

“…However, although acid-resistant vesicles (acritarchs) of inferred eukaryote origin are known from 1.8 Ga and became moderately diverse in nearshore habitats by 1.45 Ga (Lamb et al 2009), overall the midProterozoic record is very limited. Some researchers attribute this to evolutionary stasis in the marine realm during the 'boring billion', when high levels of hydrogen sulphide, which is toxic to eukaryotes, inhibited their evolutionary radiation , and latterly to the concept that major evolutionary innovations may have mostly been taking place on land at this time (Blank 2013;Wellman & Strother 2015).…”

High Molybdenum availability for evolution in a Mesoproterozoic lacustrine environment

“…The data have been used particularly to infer the record of availability of nutrients in the ocean to allow the expansion of N-fixing cyanobacteria and the diversification of eukaryotic life 1,5,[8][9][10] . However, growing evidence for the importance of shallow marine or terrestrial environments to the development of both N fixers and eukaryotes [11][12][13][14] requires an assessment of nutrient availability to the Mesoproterozoic surficial environment. Molybdenum is a key element limiting life in lakes, especially through control of N-fixation [15][16][17][18] .…”

The fitness of the environments of air and water for photosynthesis, growth, reproduction and dispersal of photoautotrophs: An evolutionary and biogeochemical perspective

“…Prokaryotic photoautotrophy appeared at least 2.4 Ga (Rasmussen et al, 2008) but perhaps as early as 3.0 to 2.6 Ga (Blank, 2013). Eukaryotic algae may have evolved as early as 2.3 to 2.0 Ga (Blank, 2013). Interestingly, the earliest cyanobacteria probably evolved in freshwaters (Blank and Sanchez-Baracaldo, 2010) and the same may also be true of the earliest photosynthetic eukaryotes (Blank, 2013).…”

“…The characteristics or 'fitness' sensu Henderson (1924) of the abiotic environment will have had a major effect on the evolutionary trajectory of life. Prokaryotic photoautotrophy appeared at least 2.4 Ga (Rasmussen et al, 2008) but perhaps as early as 3.0 to 2.6 Ga (Blank, 2013). Eukaryotic algae may have evolved as early as 2.3 to 2.0 Ga (Blank, 2013).…”