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Varona, N. S.

Publications and source records attributed to Varona, N. S..

3 recordsLinked to original sources

Bacteriophage replication strategies are associated with organic matter energy content on coral reefs

Bacteriophages, viruses that infect bacteria, play a crucial role in carbon cycling within marine environments. In coral reefs, dissolved organic matter (DOM) released by benthic primary producers such as algae fuels heterotrophic microbial growth, which can be detrimental to corals. While this microbialization process has been associated with the abundance and replication strategies of bacteriophages, the direct relationship between reef DOM composition and bacteriophage communities remains unclear. Here, we combine metabolomics, metagenomes, and viromes to demonstrate that phage abundances have significant relationships with DOM composition on the reefs of Curacao, Southern Caribbean. By constructing co-occurrence networks between free or cell-associated viruses and exometabolites, we identified thousands of statistically significant associations between phages and organic compounds. While total viral abundances did not significantly correlate with overall dissolved organic carbon (DOC) concentration, cell-associated phages had significantly more positive associations with compounds that had a reduced nominal oxidative state of carbon (NOSC). Furthermore, temperate phages were more frequently correlated with metabolites exhibiting higher Gibbs energy than lytic phages. Six of the ten viruses with the highest number of positive associations with metabolites were temperate (i.e., encoded an integrase or were identified as a prophage), despite this network consisting of approximately 90% lytic viruses. These temperate viruses were predicted to infect members of the genus Sphingobium. Together, these findings reveal a connection between phage replication strategies and DOM energy availability with potential implications for coral reef biogeochemistry. SignificanceCoral reefs are highly dynamic ecosystems where microbial communities and organic matter cycles are intricately linked. This study provides new insights into how bacteriophages interact with dissolved organic matter (DOM) composition, revealing that cell-associated bacteriophages, particularly temperate phages, are associated with more energy-rich organic compounds. These findings suggest that DOM may have a bottom-up influence on the lysis-lysogeny decision of temperate phages infecting their host or that lysogeny may play an underappreciated role in shaping the reef carbon cycle. Energy-rich organic compounds have generally been associated with increased algal abundances and coral decline. By demonstrating significant connections between viral infection strategies and the energy content of DOM, our results highlight the potential for phages to influence coral reef biogeochemistry and health.

microbiology↗

Viral and bacterial traits associated with the success of the yellow pencil coral, Madracis mirabilis, in Curacaos coral reefs

Coral reefs have experienced extensive coral loss and shifts in community composition worldwide. Despite this, some coral species appear naturally more resistant, such as Madracis mirabilis (herein Madracis). Madracis has emerged as the dominant hard coral in Curacao, comprising 26% of coral cover in reefs that declined by 78% between 1973 and 2015. Although life history traits and competitive mechanisms contribute to Madracis success, these factors alone may not fully explain it, as other species with similar traits have not shown comparable success. Here, we investigated the potential role of microbial communities in the success of Madracis on Curacao reefs by leveraging a low-bias bacterial and viral enrichment method for metagenomic sequencing of coral samples, resulting in 77 unique bacterial metagenome-assembled genomes and 2,820 viral genomic sequences. Our analyses showed that Madracis-associated bacterial and viral communities are 1.24-fold and 1.61-fold richer than the communities of five sympatric coral species combined. The Madracis-associated bacterial community was dominated by Ruegeria and Sphingomonas, genera that have previously been associated with coral health, defense against pathogens, and bioremediation. The viral community exhibited a 50% enrichment of proviruses relative to the viral communities of other corals. These proviruses have the genomic capacity to laterally transfer genes involved in antibiotic resistance, central metabolism, and oxidative stress responses, potentially enhancing the adaptive capacity of the Madracis microbiome and contributing to Madracis success on Curacaos reefs. IMPORTANCEUnderstanding why some coral species persist and thrive while most are in fast decline is critical. Madracis mirabilis is increasingly dominant on degraded reefs in Curacao, yet the role of microbial communities in its success remains underexplored. This study highlights the potential role of Madracis-associated bacterial and viral communities in supporting coral resilience and competitive success. By identifying key microbial partners and viral genes that may enhance host stress tolerance and defense against pathogens, we broaden the understanding of how the coral holobiont contributes to species persistence under environmental stress. These insights are valuable for predicting reef community shifts in a changing climate and open avenues for microbiome-informed strategies to support coral conservation and restoration.

microbiology↗

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. Bacteriophages are the most abundant and diverse members of these communities, yet very little is known about their functions in the holobiont due to 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 which increased bacterial and viral recovery in coral metagenomes by 9-fold and 3-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 Virome Database of over 20,000 viral genomes and genome fragments spanning four viral realms. The tailed bacteriophage families Kyanoviridae and Ackermannviridae were the most abundant, replacing the since-abolished groups Podoviridae and Siphoviridae. 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 eavesdrop and modulate bacterial quorum sensing, interfere with sulfur cycling, and direct molecular interactions with eukaryotic cells through the release of extracellular effectors. This study reveals the basis of bacteriophage roles in modulating ecological interactions not only among bacterial community members but also directly affecting tripartite interactions with the coral host and its endosymbiotic algae.

genomics↗