A bacterium predatory on cyanobacteria from biological soil crusts

Julie Bethany Rakes

Predatory bacteria constitute a guild of heterotrophs specialized in obtaining resources for growth from the live bacteria they prey upon. Its members have been isolated from many environments and are phylogenetically diverse, each having evolved their mode of life independently. We report on a novel type of obligatory predatory bacterium, Candidatus Cyanoraptor togatus, belonging to the Chitinophagaceae family (Bacteroidetes phylum) that attacks filamentous cyanobacteria in soils, including Microcoleus vaginatus, the most abundant terrestrial cyanobacterium, and can demonstrably bring about catastrophic mortality events to their populations in nature and in production facilities. A polyphasic study combining confocal and electron microscopy, cultivation in co-culture with its prey, genomic analyses and physiological assays reveal that this organism sustains a complex life cycle, with submicrometer, non-growing, non-motile, internally compartmentalized coccoid propagules that gain attachment and entry into the prey’s cytoplasmatic space, where they hydrolyze its contents, growing into bacilloid and eventually pseudofilamentous forms, which then undergo multiple divisions and excretion of extracellular vesicles to form new propagule cells. Its type strain, LGM-1T, has a 3.3 Mbp genome, is rich in hydrolase-encoding genes endowed with signal peptides for excretion and notoriously deficient in pathways for amino acid biosynthesis. Physiologically, the propagule cells are quite vulnerable to environmental stressors, likely curtailing its success in natural systems. While no close relatives exist in culture, 16S rRNA sequences with affinities to this organism are found in molecular surveys from a variety of environments.