Genomic and induction evidence for bacteriophage contributions to sargassum-bacteria symbioses.

BACKGROUND: Symbioses between primary producers and bacteria are crucial for nutrient exchange that fosters host growth and niche adaptation. Yet, how viruses that infect bacteria (phages) influence these bacteria-eukaryote interactions is still largely unknown. Here, we investigate the role of viruses on the genomic diversity and functional adaptations of bacteria associated with pelagic sargassum. This brown alga has dramatically increased its distribution range in the Atlantic in the past decade and is predicted to continue expanding, imposing severe impacts on coastal ecosystems, economies, and human health. RESULTS: We reconstructed 73 bacterial and 3963 viral metagenome-assembled genomes (bMAGs and vMAGs, respectively) from coastal Sargassum natans VIII and surrounding seawater. S. natans VIII bMAGs were enriched in prophages compared to seawater (28% and 0.02%, respectively). Rhodobacterales and Synechococcus bMAGs, abundant members of the S. natans VIII microbiome, were shared between the algae and seawater but were associated with distinct phages in each environment. Genes related to biofilm formation and quorum sensing were enriched in S. natans VIII phages, indicating their potential to influence algal association in their bacterial hosts. In-vitro assays with a bacterial community harvested from sargassum surface biofilms and depleted of free viruses demonstrated that these bacteria are protected from lytic infection by seawater viruses but contain intact and inducible prophages. These bacteria form thicker biofilms when growing on sargassum-supplemented seawater compared to seawater controls, and phage induction using mitomycin C was associated with a significant decrease in biofilm formation. The induced metagenomes were enriched in genomic sequences classified as temperate viruses compared to uninduced controls. CONCLUSIONS: Our data shows that prophages contribute to the flexible genomes of S. natans VIII-associated bacteria. These prophages encode genes with symbiotic functions, and their induction decreases biofilm formation, an essential capacity for flexible symbioses between bacteria and the alga. These results indicate that prophage acquisition and induction contribute to genomic and functional diversification during sargassum-bacteria symbioses, with potential implications for algae growth. Video Abstract.

Globally distributed bacteriophage genomes reveal mechanisms of tripartite phage-bacteria-coral interactions.

Reef-building corals depend on an intricate community of microorganisms for functioning and resilience. The infection of coral-associated bacteria by bacteriophages can modify bacterial ecological interactions, yet very little is known about phage functions in the holobiont. This gap stems from methodological limitations that have prevented the recovery of high-quality viral genomes and bacterial host assignment from coral samples. Here, we introduce a size fractionation approach that increased bacterial and viral recovery in coral metagenomes by 9-fold and 2-fold, respectively, and enabled the assembly and binning of bacterial and viral genomes at relatively low sequencing coverage. We combined these viral genomes with those derived from 677 publicly available metagenomes, viromes, and bacterial isolates from stony corals to build a global coral virus database of over 20,000 viral genomic sequences spanning four viral realms. The tailed bacteriophage families Kyanoviridae and Autographiviridae were the most abundant, replacing groups formerly referred to as Myoviridae and Podoviridae, respectively. Prophage and CRISPR spacer linkages between these viruses and 626 bacterial metagenome-assembled genomes and bacterial isolates showed that most viruses infected Alphaproteobacteria, the most abundant class, and less abundant taxa like Halanaerobiia and Bacteroidia. A host-phage-gene network identified keystone viruses with the genomic capacity to modulate bacterial metabolic pathways and direct molecular interactions with eukaryotic cells. This study reveals the genomic basis of nested symbioses between bacteriophage, bacteria, and the coral host and its endosymbiotic algae.

Snow viruses and their implications on red snow algal blooms.

Algal blooms can give snowmelt a red color, reducing snow albedo and creating a runaway effect that accelerates snow melting. The occurrence of red snow is predicted to grow in polar and subpolar regions with increasing global temperatures. We hypothesize that these algal blooms affect virus-bacteria interactions in snow, with potential effects on snowmelt dynamics. A genomic analysis of double-stranded DNA virus communities in red and white snow from the Whistler region of British Columbia, Canada, identified 792 putative viruses infecting bacteria. The most abundant putative snow viruses displayed low genomic similarity with known viruses. We recovered the complete circular genomes of nine putative viruses, two of which were classified as temperate. Putative snow viruses encoded genes involved in energy metabolisms, such as NAD+ synthesis and salvage pathways. In model phages, these genes facilitate increased viral particle production and lysis rates. The frequency of temperate phages was positively correlated with microbial abundance in the snow samples. These results suggest the increased frequency of temperate virus-bacteria interactions as microbial densities increase during snowmelt. We propose that this virus-bacteria dynamic may facilitate the red snow algae growth stimulated by bacteria.IMPORTANCEMicrobial communities in red snow algal blooms contribute to intensifying snowmelt rates. The role of viruses in snow during this environmental shift, however, has yet to be elucidated. Here, we characterize novel viruses extracted from snow viral metagenomes and define the functional capacities of snow viruses in both white and red snow. These results are contextualized using the composition and functions observed in the bacterial communities from the same snow samples. Together, these data demonstrate the energy metabolism performed by viruses and bacteria in a snow algal bloom, as well as expand the overall knowledge of viral genomes in extreme environments.

The coral microbiome in sickness, in health and in a changing world.

Stony corals, the engines and engineers of reef ecosystems, face unprecedented threats from anthropogenic environmental change. Corals are holobionts that comprise the cnidarian animal host and a diverse community of bacteria, archaea, viruses and eukaryotic microorganisms. Recent research shows that the bacterial microbiome has a pivotal role in coral biology. A healthy bacterial assemblage contributes to nutrient cycling and stress resilience, but pollution, overfishing and climate change can break down these symbiotic relationships, which results in disease, bleaching and, ultimately, coral death. Although progress has been made in characterizing the spatial-temporal diversity of bacteria, we are only beginning to appreciate their functional contribution. In this Review, we summarize the ecological and metabolic interactions between bacteria and other holobiont members, highlight the biotic and abiotic factors influencing the structure of bacterial communities and discuss the impact of climate change on these communities and their coral hosts. We emphasize how microbiome-based interventions can help to decipher key mechanisms underpinning coral health and promote reef resilience. Finally, we explore how recent technological developments may be harnessed to address some of the most pressing challenges in coral microbiology, providing a road map for future research in this field.

Viruses of sulfur oxidizing phototrophs encode genes for pigment, carbon, and sulfur metabolisms.

Viral infections modulate bacterial metabolism and ecology. Here, we investigated the hypothesis that viruses influence the ecology of purple and green sulfur bacteria in anoxic and sulfidic lakes, analogs of euxinic oceans in the geologic past. By screening metagenomes from lake sediments and water column, in addition to publicly-available genomes of cultured purple and green sulfur bacteria, we identified almost 300 high and medium-quality viral genomes. Viruses carrying the gene psbA, encoding the small subunit of photosystem II protein D1, were ubiquitous, suggesting viral interference with the light reactions of sulfur oxidizing autotrophs. Viruses predicted to infect these autotrophs also encoded auxiliary metabolic genes for reductive sulfur assimilation as cysteine, pigment production, and carbon fixation. These observations show that viruses have the genomic potential to modulate the production of metabolic markers of phototrophic sulfur bacteria that are used to identify photic zone euxinia in the geologic past.