Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust

Biological soil crusts (biocrusts) are photosynthetic hot spots in deserts and cover similar to 12% of the Earth's terrestrial surface, and yet they face an uncertain future given expected shifts in rainfall events. Laboratory wetting of biocrust communities is known to cause a bloom of Firmicutes which rapidly become dominant community members within 2 days after emerging from a sporulated state. We hypothesized that their bacteriophages (phages) would respond to such a dramatic increase in their host's abundance. In our experiment, wetting caused Firmicutes to bloom and triggered a significant depletion of cyanobacterial diversity. We used genome-resolved metagenomics to link phage to their hosts and found that the bloom of the genus Bacillus correlated with a dramatic increase in the number of Caudovirales phages targeting these diverse spore-formers (r = 0.762). After 2 days, we observed dramatic reductions in the relative abundances of Bacillus, while the number of Bacillus phages continued to increase, suggestive of a predator-prey relationship. We found predicted auxiliary metabolic genes (AMGs) associated with sporulation in several Caudovirales genomes, suggesting that phages may influence and even benefit from sporulation dynamics in biocrusts. Prophage elements and CRISPR-Cas repeats in Firmicutes metagenome-assembled genomes (MAGs) provide evidence of recent infection events by phages, which were corroborated by mapping viral contigs to their host MAGs. Combined, these findings suggest that the blooming Firmicutes become primary targets for biocrust Caudovirales phages, consistent with the classical kill-the-winner hypothesis. IMPORTANCE This work forms part of an overarching research theme studying the effects of a changing climate on biological soil crust (biocrust) in the Southwestern United States. To our knowledge, this study was the first to characterize bacteriophages in biocrust and offers a view into the ecology of phages in response to a laboratory wetting experiment. The phages identified here represent lineages of Caudovirales, and we found that the dynamics of their interactions with their Firmicutes hosts explain the collapse of a bacterial bloom that was induced by wetting. Moreover, we show that phages carried host-altering metabolic genes and found evidence of proviral infection and CRISPR-Cas repeats within host genomes. Our results suggest that phages exert controls on population density by lysing dominant bacterial hosts and that they further impact biocrust by acquiring host genes for sporulation. Future research should explore how dominant these phages are in other biocrust communities and quantify how much the control and lysis of blooming populations contributes to nutrient cycling in biocrusts.