Cyanobacteria Evolution Insight from the Fossil Record

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Cyanobacteria Evolution Insight from the Fossil Record Free Radical Biology and Medicine 140 (2019) 206–223 Contents lists available at ScienceDirect Free Radical Biology and Medicine journal homepage: www.elsevier.com/locate/freeradbiomed Cyanobacteria evolution: Insight from the fossil record T ∗ Catherine F. Demoulina, ,1, Yannick J. Laraa,1, Luc Corneta,b, Camille Françoisa, Denis Baurainb, Annick Wilmottec, Emmanuelle J. Javauxa a Early Life Traces & Evolution - Astrobiology, UR ASTROBIOLOGY, Geology Department, University of Liège, Liège, Belgium b Eukaryotic Phylogenomics, InBioS-PhytoSYSTEMS, University of Liège, Liège, Belgium c BCCM/ULC Cyanobacteria Collection, InBioS-CIP, Centre for Protein Engineering, University of Liège, Liège, Belgium ARTICLE INFO ABSTRACT Keywords: Cyanobacteria played an important role in the evolution of Early Earth and the biosphere. They are responsible Biosignatures for the oxygenation of the atmosphere and oceans since the Great Oxidation Event around 2.4 Ga, debatably Cyanobacteria earlier. They are also major primary producers in past and present oceans, and the ancestors of the chloroplast. Evolution Nevertheless, the identification of cyanobacteria in the early fossil record remains ambiguous because the Microfossils morphological criteria commonly used are not always reliable for microfossil interpretation. Recently, new Molecular clocks biosignatures specific to cyanobacteria were proposed. Here, we review the classic and new cyanobacterial Precambrian biosignatures. We also assess the reliability of the previously described cyanobacteria fossil record and the challenges of molecular approaches on modern cyanobacteria. Finally, we suggest possible new calibration points for molecular clocks, and strategies to improve our understanding of the timing and pattern of the evolution of cyanobacteria and oxygenic photosynthesis. 1. Introduction eukaryote [8,9], and subsequent higher-order endosymbiotic events [10]. The endosymbiotic theory is well supported by biochemical, ul- Modern cyanobacteria constitute an ancient and well-diversified trastructural, ecological and molecular data [11], although the identity bacterial phylum, with unique complex morphologies and cellular dif- and habitat of the cyanobacterial ancestor of the chloroplast are still ferentiation. They play a key role in food webs as primary producers debated [12–17]. performing oxygenic photosynthesis. Cyanobacteria also played a major Despite the importance of cyanobacteria in the early evolution of role in early biogeochemical fluxes and in Life and Earth evolution. Earth and life, fundamental questions remain about their origin, the They are the only prokaryotic organisms that perform oxygenic pho- timing and pattern of their diversification, and the origin of oxygenic tosynthesis, and are thus generally held responsible for the rise of photosynthesis, ranging from the Archean to the GOE [18]. One crucial oxygen in the atmosphere and oceans around 2.4 Ga, during the so- problem to solve is the discrepancy between the unambiguous cyano- called Great Oxidation Event (GOE [1,2]), facilitated by geological bacterial fossil record, starting at 1.9 Ga, the GOE at 2.4 Ga, and the processes [3]. Oxygenic photosynthesis has enabled the oxygenation of report of several older geochemical data suggestive of oxygenic pho- oceanic and terrestrial niches, and the diversification of complex life tosynthesis ([19]; but see Ref. [20]) [21–25]; and [26,27]. [4]. Indeed, most modern eukaryotes need a minimal concentration of Several types of evidence are used to reconstruct the fossil record of molecular oxygen to synthesize their sterol membranes [5]. They di- cyanobacteria, but all have their limitations and challenges. versified from a last eukaryotic common ancestor (LECA), an aerobe Stromatolites are usually associated to cyanobacterial activity. protist with a mitochondrion [6]. Further increased oxygen con- However, although conical stromatolites seem to plead for oxygenic centration was required for the metabolic activity of mobile macro- photosynthesis [28], others types of stromatolites and microbially in- scopic metazoans [7]. At least 1.05 Ga ago, oxygenic photosynthesis duced sedimentary structures (MISS) [29–31] may have been produced spread among some eukaryotic clades, giving rise to diverse types of by non-cyanobacterial lineages, such as anoxygenic phototrophs algae and later to plants. This important evolutionary step was due to [28,32], or by/in association with methanotrophs [33]. This suggests the primary endosymbiosis of a cyanobacterium within a unicellular that stromatolites and MISS are not necessarily indicative of ∗ Corresponding author. E-mail address: [email protected] (C.F. Demoulin). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.freeradbiomed.2019.05.007 Received 29 November 2018; Received in revised form 13 March 2019; Accepted 5 May 2019 Available online 09 May 2019 0891-5849/ © 2019 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). C.F. Demoulin, et al. Free Radical Biology and Medicine 140 (2019) 206–223 cyanobacteria activity, and perhaps not even of photosynthesis [34]. 2.1. Morphology and division pattern Biomarkers (fossil molecules) can indicate the presence of metabolisms such as oxygenic photosynthesis, but they are preserved only in well- Cyanobacteria were traditionally described as algae and referred to preserved unmetamorphosed rocks, and contamination is a challenge as ‘Cyanophyta’ or ‘Blue green algae’. Until the end of the 20th century, [35]. Among those, lipids such as 2-methyl-hopanes are produced by the nomenclatural system of cyanobacteria followed the International cyanobacteria [36] but not only [37], and pigments such as porphyrins Code of Botanical Nomenclature. In the late seventies, Stanier and with N isotope composition [38]. Other geochemical (redox and iso- colleagues [44] recognized the prokaryotic nature of the cyanobacteria topic) proxies can also inform on the presence of molecular oxygen in and proposed to follow the International Code of Nomenclature for the water column or biologically-induced isotopic fractionation due to Bacteria. According to the Bergey's Manual of Systematic Bacteriology, oxygenic photosynthesis, but their interpretation is often debated. Fi- and following the Stanier approach and Rippka et al. (1979) [45] nally, microfossils may provide direct evidence for cyanobacteria, but concepts, cyanobacteria were divided into two groups: unicellular and their identification is often ambiguous. At the present time, thecya- multicellular filamentous cyanobacteria; and five subsections based on nobacterial identity of only three fossil taxa is not debated: Eoento- morphological criteria, and corresponding to five former cyanobacterial physalis, Eohyella and Polybessurus. Eoentophysalis belcherensis is the orders: Chroococcales (section I) and Pleurocapsales (section II) harbor oldest microfossil interpreted with certainty as a cyanobacterium [39]. unicellular cells, which divide by binary fission in one or multiple plans This microfossil has been described from 1.89–1.84 Ga silicified stro- and are solitary or arranged in colonies. Pleurocapsales can also pro- matolites of the Belcher Supergroup, Hudson Bay, Canada [39]. duce small easily dispersed cells (baeocytes) after division by multiple Microbiology of modern cyanobacteria pairs the geological and fissions. Within the multicellular filamentous cyanobacteria, Oscilla- paleobiological approaches. The accumulation of modern cyano- toriales (section III) have only vegetative cells arranged in filaments, bacterial genetic data in public databases increasingly allows phylo- whereas Nostocales (section IV), and Stigonematales (section V) are genetic reconstructions and molecular clock analyses aimed at esti- capable of producing specialized cells, the heterocytes, which allow N- mating the origin of the phylum and the origin of oxygenic fixation in an anoxic compartment; or can exhibit environmental stress photosynthesis. However, due to the lack of tree calibrations from the resistant cells called akinetes. Besides, cyanobacteria from section V are fossil record, contamination of genetic sequences, chosen dataset, and also characterized by their ability to divide in more than one plane and limitations or differences in models, these estimates are quite variable form true branched trichomes [45]. [40]. Thus, discrepancies between the geological and fossil records and Since that time, the taxonomic classification of cyanobacteria has molecular phylogenies remain, and the origin and evolution of cyano- been continually reevaluated with the development of electron micro- bacteria, oxygenic photosynthesis, and the chloroplast are still debated. scopy and genetic characterization methods [46]. The classification In this paper, we review classic and new biosignatures of cyano- into subsections is practical but does not reflect phylogeny because they bacteria, critically assess their fossil record, and suggest possible new are not all monophyletic except for the Nostocales and Stigonematales. calibration points for molecular clocks. We also briefly discuss mole- Interpreting microfossils as cyanobacteria is generally based on cular phylogenies, molecular clocks and their discrepancies. We finally morphological criteria, and their mode of division. However, the simple make some suggestions for future research, to improve our under-
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