Deciphering Primordial Cyanobacterial Genome Functions from Protein Network Analysis

• Published in: Current biology Vol. 25; no. 5; pp. 628 - 634
• Main Authors: Harel, Arye, Karkar, Slim, Cheng, Shu, Falkowski, Paul G., Bhattacharya, Debashish
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 02-03-2015
• Subjects: Bacteria, Anaerobic - genetics; Computational Biology; Cyanobacteria - genetics; Evolution, Molecular; Genome, Bacterial - genetics; Hydrogenase - genetics; Multigene Family - genetics; Oxidation-Reduction; Photosynthesis - genetics; Protein Interaction Maps - genetics; Proteomics - methods; Species Specificity
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2014.12.061

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.
•Network analysis elucidates ancient connections between different redox lifestyles•Cyanobacteria and obligate anaerobes share the most core gene families•Ancestral cyanobacterial functions include photosynthesis, hydrogenase, and defense•Network analysis allows exploration of RC origin and evolution in bacterial lineages
The origin of oxygenic cyanobacteria, over 2.5 billion years ago, is poorly understood. Harel et al. use network analysis to elucidate the position of cyanobacteria as an evolutionary bridge between anaerobic and obligate aerobic prokaryotes. They identify ancient cyanobacterial genome traits and explore the history of photosynthesis in microbes.