Deciphering Primordial Cyanobacterial Genome Functions from Protein Network Analysis

Abstract

The Great Oxidation Event (GOE) ∼2.4 billion years ago resulted from the accumulation of oxygen by the ancestors of cyanobacteria [1-3]. Cyanobacteria continue to play a significant role in primary production [4] and in regulating the global marine and limnic nitrogen cycles [5, 6]. Relatively little is known, however, about the evolutionary history and gene content of primordial cyanobacteria [7, 8]. To address these issues, we used protein similarity networks [9], containing proteomes from 48 cyanobacteria as the test group, and reference proteomes from 84 microbes representing four distinct metabolic groups from most reducing to most oxidizing: methanogens, obligate anaerobes (nonmethanogenic), facultative aerobes, and obligate aerobes. These four metabolic groups represent extant bioinformatic proxies for ancient redox chemistries, extending from an anoxic origin through the GOE and ultimately to obligate aerobes [10-13]. Analysis of the network metric degree showed a strong relationship between cyanobacteria and obligate anaerobes, from which cyanobacteria presumably arose, for core functions that include translation, photosynthesis, energy conservation, and environmental interactions. These data were used to reconstruct primordial functions in cyanobacteria that included nine gene families involved in photosynthesis, hydrogenases, and proteins involved in defense from environmental stress. The presence of 60% of these genes in both reaction center I (RC-I) and RC-II-type bacteria may be explained by selective loss of either RC in the evolutionary history of some photosynthetic lineages. Finally, the network reveals that cyanobacteria occupy a unique position among prokaryotes as a hub between anaerobes and obligate aerobes.

Early emergence of the FtsH proteases involved in photosystem II repair

“…However, recent detailed analysis of the phylogeny of RC proteins indicates that HGT of RCs to an ancestral nonphotosynthetic cyanobacterium from anoxygenic phototrophic bacteria is unlikely (Cardona 2016b); furthermore, the evolution of RC proteins shows that the last common ancestor to all phototrophic bacteria had already evolved Type I and Type II RC proteins from an earlier gene duplication event (Sousa et al 2013, Harel et al 2015. In addition, it has been argued that the evolution of the structural complexity of PSII and the origin of the oxygenevolving manganese cluster can only be explained if both types of RC had been evolving in cooperation since the dawn of photosynthesis and that water oxidation might therefore have occurred at a far earlier stage of evolution that previously thought (Cardona 2016b(Cardona , 2017.…”

“…In contrast, more recent phylogenetic analyses have led to the suggestion that the evolution of Type I and Type II RCs might have occurred in a single organism after a gene duplication event (Mulkidjanian et al 2006, Sousa et al 2013, Harel et al 2015 and, possibly, that Type I and Type II RCs might have then been transferred at various stages of evolution to other types of nonphotosynthetic bacteria through horizontal gene transfer (HGT) (Mulkidjanian et al 2006). Given the fact that the geochemical record of photosynthesis dates back to 3.5 to 3.8 billion years ago, such 'gene duplication' hypotheses raise the possibility that oxygenic photosynthesis might have evolved much earlier than previously thought, perhaps hundreds of millions of years before the Great Oxidation Event (Lyons et al 2014).…”

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

“…However, lines of evidence from extant organismal physiology and Precambrian geochemical indicators corroborate the possibility that some rise in oxygen or other oxidized chemical species preceded the emergence of Form I Rubisco enzymes within cyanobacterial clades. Previous phylogenetic analyses indicate that anoxygenic photosynthetic lineages are more deeply rooted than oxygenic cyanobacterial lineages (Mulkidjanian et al., 2006; Xiong, 2007) and that cyanobacteria represent an evolutionary intermediate between anaerobic and obligate aerobic organisms (Harel, Karkar, Cheng, Falkowski, & Bhattacharya, 2015). Co‐evolution at organismal (i.e., the emergence or development of localized CO 2 or O 2 control volumes within cells) and protein (i.e., direct accumulation of mutations in sequences representing oxygen‐sensitive regions of proteins) levels may have been tightly coupled just prior to the GOE due to oxygen stresses and diminishing CO 2 availability in the near‐surface environment (Knoll, 2006; Tomitani et al., 2006).…”

Photosystem II is a Chimera of Reaction Centers

“…This interpretation is in conflict with phylogenomic data, which consistently do not locate cyanobacteria as a particularly early branch in comparison with other phototrophic groups (Ciccarelli et al 2006;Segata et al 2013;Marin et al 2016). Therefore, the evidence at hand (Mulkidjanian et al 2006;Sousa et al 2013;Harel et al 2015) might be better reinterpreted as evidence for two distinct reaction centers as a trait of the ancestral populations of photosynthetic bacteria. Today, this trait is retained, not acquired, in cyanobacteria.…”

“…Firstly, the evolution of the chlorophyll synthesis pathway suggests that Type I and Type II reaction centers originated from an ancestral gene duplication event (Sousa et al 2013); secondly, proteome similarity networks of a diverse group of prokaryotes provided a similar result (Harel et al 2015). But earlier genome comparisons had lent support to the hypothesis that the last common ancestor to all photosynthetic organisms had already evolved two distinct reaction centers from an early gene duplication event (Mulkidjanian et al 2006).…”