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Hold the salt: Freshwater origin of primary plastids
Wednesday, 2017/09/13 | 08:47:09
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PNAS Sept 12 2017
The evolution of oxygenic photosynthesis by cyanobacteria was arguably one of the most significant biological events in Earth’s history, shaping the atmosphere and subsequently leading to diverse ecosystems (1). The permanent endosymbiotic merger between a cyanobacterium and a unicellular heterotrophic eukaryote in deep evolutionary time set the stage for the stunning diversity of photosynthetic eukaryotes and ecosystems seen today, giving rise to the supergroup Archaeplastida, the red, glaucophyte, and green algae and their descendent land plants. Later transfers of photosynthesis to other lineages of heterotrophic eukaryotes through eukaryote–eukaryote mergers (secondary and tertiary endosymbiosis) led to many near-shore and open-ocean species, including kelps, diatoms, coccolithophors, and dinoflagellates (2). The cyanobacterial ancestry of primary plastids is no longer debated, but the precise donor of primary plastids, the timing and ecological context of the merger, and modifications since the event have received much attention (3⇓⇓–6). In PNAS, Sánchez-Baracaldo et al. (7) examine the evolution of primary photosynthesis and its habitat of origin using the most comprehensive dataset thus far from photosynthetic cyanobacteria and eukaryotes.
Reconstructing the history of primary endosymbiosis is challenging due to its deep evolutionary time and long separation of descendent lineages. The oldest eukaryotic fossils (about 1.7 billion y ago) cannot be unequivocally assigned and most of the age constraints used for time-tree analyses are from Phanerozoic fossils. All three lineages of Archaeplastida possess primary plastids of cyanobacterial origin but, as seen from newly abundant plastid genomic data from diverse photosynthetic eukaryotes, each group has evolved distinct modifications of the inherited cyanobacterial genetic “toolkit” for plastid functions, with independent gene losses and transfers to the host nucleus of plastid targeted genes, thus solidifying the integration (3, 8, 9). Likewise, free-living cyanobacteria further diversified since their cousins participated in primary endosymbiosis. Alternative candidates for the sister group to Archaeplastida plastids range from among morphologically simple, early-diverging (6) to more derived and morphologically complex cyanobacteria (5), to the possibility that primary plastids of Archaeplastida have multiple origins (10, 11).
Two exciting discoveries of novel and deeply diverging lineages of cyanobacteria and green algae, as well as growing availability of genomic data from diverse photosynthetic species, prompted a reinvestigation of these fundamental questions. The recent discovery of Gloeomargarita lithophora, a cyanobacterium found in microbiolites of alkaline lakes in Mexico, made a splash because this species is among the early-diverging cyanobacterial lineages and is implicated as the closest relative to Archaeplastida (6). Second, an early-diverging lineage comprising the marine deep-water green algae Palmophyllum and Verdigellas was determined from analysis of plastid genome data (12).
Sánchez-Baracaldo et al. (7) analyzed multiple sources of existing plastid and bacterial genomic data, including that of the new species mentioned above, to address scenarios and timing for the evolution of primary endosymbiosis leading to the first photosynthetic eukaryotes and explicitly tested the freshwater origin of primary plastid lineages using ancestral state reconstruction of habitat data. Significantly, their study resolved the newly discovered cyanobacterium Gloeomargarita as the closest living relative to Archaeplastida and revealed a freshwater origin of primary endosymbiosis between cyanobacteria and eukaryotes (4, 6), with divergence of Gloeomargarita from the most recent ancestor of Archaeplastida at 2.1 billion y ago (Fig. 1). Thus, plastids evolved from among the early-diverging, small, unicellular cyanobacteria before the emergence of larger unicellular and filamentous forms that likely correspond to the first recognizable fossil cyanobacteria. Their analyses provided a mean age of diversification of green algae and red algae that is older than the fossil red Bangiomorpha (1.1 billion y ago). Given the freshwater ancestry of Archaeplastida, marine algae appear only in the late Proterozoic. Extant Archaeplastida groups include marine and freshwater species, but there is a growing appreciation for the prevalence and diversity of freshwater, terrestrial, and even aeroterrestrial taxa (13, 14), and 1-billion-y-old shales containing fossil eukaryotes have been interpreted as ancient freshwater lake beds (15). Sánchez-Baracaldo et al. (7) also reinforce the later (Neoproterozoic) timing of an independent primary endosymbiosis within the Rhizaria. The amoeba Paulinella has blue-green inclusions that were initially interpreted as intracellular symbiotic cyanobacteria but were later shown to be permanent plastids of cyanobacterial origin from among the alpha-cyanobacteria, a lineage distinct from the source of plastids in the Archaeplastida, the beta-cyanobacteria
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