New life for old discovery: amazing story about how bacterial predation on Chlorella resolved a paradox of dark cyanobacteria and gave the key to early history of oxygenic photosynthesis and aerobic respiration

Abstract

chlorophyll-less bacterium Vampirovibrio chlorellavorus attacking Chlorella vulgaris and described its morphology and life cycle, although misattributed it to the phylum Proteobacteria. Over four decades, freeze-dried samples of infected Chlorella have been stored in oblivion, until in the early 2010s “proteobacterial” predator was reattributed to the phylum Cyanobacteria. V. chlorellavorus , the type species of the order Vampirovibrionales within the class Vampirovibrionia became the first, and to date unique cultured “dark” (non-photosynthetic, chlorophyll-less) cyanobacterium in contrast to “light” (photosynthetic, chlorophyll-containing) members of the class Oxyphotobacteria that habitually encompassed the phylum Cyanobacteria. Thus, taxonomic reattribution of V. chlorellavorus confirmed the early suggestions that cyanobacteria (blue-green algae) were not only photosynthetic microorganisms. Consequent metagenomic studies have extended the described diversity of dark cyanobacteria: besides Vampirovibrionales, the class Vampirovibrionia was shown to contain the orders Gastranaerophilales, Obscuribacterales, and Caenarcanales embracing metabolically diverse species with different lifestyles from development in ground water to obligate symbiosis with microalgae and oxymonad protists. Metagenomic research of dark cyanobacteria over the past decade elicited three phyla sibling to Cyanobacteria – Blackallbacteria (former Sericytochromatia), Margulisbacteria, and Saganbacteria. Comparative analysis and annotation of their metagenome-assembled genomes (MAGs) revived the discussion on the origin of oxygenic photosynthesis and aerobic respiration, primarily focusing at dilemma “dark cyanobacteria: primordial or late”. Thus, besides opening separate page in research of symbioses between protists and bacteria, and apart from looking deeper into diversity of cyanobacteria, the discovery of V. chlorellavous got a new life within evolutionary biology mainstream.