Gloeobacter and the implications of a freshwater origin of Cyanobacteria

Abstract

The earliest branching cyanobacterium, Gloeobacter, exhibits a number of ancestral traits including the lack of thylakoids. It occurs epilithically in microbial mats, both subaerially and submerged in low-salinity habitats. These habitats and the absence of thylakoids are associated with the occurrence of membraneassociated photosynthetic processes in the plasma membrane, possibly limiting the rate of both assembly and reassembly of the oxygen-evolving complex, as well as the photosynthetic rate and in vitro growth rate. These factors interact with the occurrence of Gloeobacter in mats to constrain productivity in nature. Traits found in living Gloeobacter, with the probable time of origin of oxygenic photosynthesis and diversification of cyanobacteria, can be related to the possible role of oxygenic primary productivity and organic carbon burial on land during the early Earth in low-salinity environments around the time of the global oxidation event.

Lack of Fe(II) transporters in basal Cyanobacteria complicates iron uptake in ferruginous Archean oceans

“…Significantly, soluble Fe(II) was oxidized to barely soluble Fe(III) in the photosynthetically active top layers of aquatic environments, suggesting that early life had to evolve means to overcome iron limitation. Our hypothesis was that, given a continuous lineage, the handful of basal taxa of ancient Cyanobacteria that left modern-day descendants would have retained some ancestral features (Raven and Sánchez-Baracaldo, 2021), with evidence of FeoB, FTR1, TonB and ExbB/D in their genetic complement prior to the GOE (Qui et al, 2021;Fresenborg et al 2020). FeoB, is considered the primary Fe(II) transporter in Cyanobacteria, based on studies of the Cyanobacterial model organism, Synechocystis sp.…”

Origin of cyanobacterial thylakoids via a non-vesicular glycolipid phase transition and their impact on the Great Oxygenation Event

“…Gloeobacter contains a homolog of Vipp1, found in all other oxygenic photosynthetic organisms (Raven and Sanchez-Baracaldo, 2021). The Vipp1 protein has been functionally associated to thylakoid biogenesis in a multitude of biological models, by various genetic, structural or biochemical studies (Mechela et al, 2019), but the precise understanding of its role, at molecular level, still remains puzzling in spite of recent advances in the resolution of its structural organization (Gupta et al, 2021).…”

“…The Vipp1 protein has been functionally associated to thylakoid biogenesis in a multitude of biological models, by various genetic, structural or biochemical studies (Mechela et al, 2019), but the precise understanding of its role, at molecular level, still remains puzzling in spite of recent advances in the resolution of its structural organization (Gupta et al, 2021). Gloeobacter Vipp1 lacks a ~30 amino acid extension found in thylakoid-containing organisms (Raven and Sanchez-Baracaldo, 2021), and this protein plays a primitive function which is still elusive. In thylakoid-containing Synechocystis or in the chloroplast of the green alga Chlamydomonas reinhardtti, vipp1 mutations lead to the formation of aberrant thylakoid convergence zones (Gupta et al, 2021;Nordhues et al, 2012).…”

“…Most ancient Cyanobacteria are likely to have populated low salinity habitats and dry environments (Blank and Sanchez-Baracaldo, 2010) as small unicellular forms close to present-day Gloeobacter (Sanchez- Baracaldo and Cardona, 2020;Mares et al, 2019;Raven and Sanchez-Baracaldo, 2021). The GOE was proposed to be the consequence of the ability of Cyanobacteria to form multicellular filaments, resembling extant Pseudanabaena, facilitating the formation of microbial mats, a feature supposed to increase their ecological dominance to such an extent that atmospheric O 2 underwent this dramatic increase (Sanchez- Baracaldo and Cardona, 2020).…”

“…Thylakoids are evidently not required for oxygenic photosynthesis since Gloeobacter hosts its photosystems in its cytoplasmic (or inner) membrane (Raven and Sanchez-Baracaldo, 2021). The evolution of thylakoids starts with the appearance of continuous linear sacks with several concentric, uninterrupted layers (Mares et al, 2019).…”