A bacterium predatory on cyanobacteria of biological soil crusts

Julie A Bethany, School of Life Sciences, Arizona State University, Tempe, AZ and Ferran Garcia-Pichel, Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, AZ

Background/Question/Methods
Biocrusts are topsoil microbial communities that can be found in drylands worldwide, providing essential ecosystem services such as fixing and releasing carbon and nitrogen, contributing to soil fertility, as well as stabilizing soils. Within these communities, cyanobacteria serve as the pioneer organisms. Due to their foundational role, most research has focused on the cyanobacteria, rather than other bacterial components. Loss factors, like predation and disease, have not received much attention, although their presence and potential importance is known. An understanding of disease agents as loss factors is needed to understand biocrust dynamics, function and health. We report on the presence of a predatory bacterium that impacts biological soil crust cyanobacteria.
Diseased biocrust areas showed cm-sized fairy-ring like clearings. To isolate potential predatory bacteria from them we used flow cytometric cell sorting. TEM (transmission electron microscopy) was used to identify this organism and to investigate its life cycle. To further characterize this predator, we used whole genome sequencing and physiological experiments. Field surveys paired with 16S rRNA gene sequencing were used to determine its incidence on biocrust community structure and worldwide distribution. Finally, exometabolite profiling is underway to identify any prey exudates that impact predatory function.

Results/Conclusions
Here we report on the discovery of an infectious pathogen, a predatory bacterium, belonging to a novel genus in the family Chitinophagaceae (Bacteriodetes). It is an obligate, intracellular pathogen specialized on filamentous non-heterocystous, highly motile cyanobacteria, that lacks major pathways for amino acid biosynthesis and motility. The predator has a dimorphic life cycle that involves an extracellular propagule phase and an intracellular replication phase. Propagules can attach to cyanobacterial filaments, and presumably spread by their movements. In-lab assays indicated that it is highly susceptible to high temperature, UV damage and desiccation, all conditions common in its natural environment. It is associated with a common symptomology, cm-sized viral-like plaques or fairy rings. The symptoms and molecular signatures have been detected from biocrust worldwide. Its presence leads to major microbial community shifts and catastrophic loss of chlorophyll and its landscape incidence can be as high as 30% of the biocrust-covered area. We discuss approaches to avoid its unintended spread in processes of biocrusts restoration.