Top‐heavy trophic structure within benthic viral dark matter

Abstract

A better understanding of system‐specific viral ecology in diverse environments is needed to predict patterns of virus–host trophic structure in the Anthropocene. This study characterised viral‐host trophic structure within coral reef benthic cyanobacterial mats—a globally proliferating cause and consequence of coral reef degradation. We employed deep longitudinal multi‐omic sequencing to characterise the viral assemblage (ssDNA, dsDNA, and dsRNA viruses) and profile lineage‐specific host–virus interactions within benthic cyanobacterial mats sampled from Bonaire, Caribbean Netherlands. We recovered 11,012 unique viral populations spanning at least 10 viral families across the orders Caudovirales, Petitvirales, and Mindivirales. Gene‐sharing network analyses provided evidence for extensive genomic novelty of mat viruses from reference and environmental viral sequences. Analysis of coverage ratios of viral sequences and computationally predicted hosts spanning 15 phyla and 21 classes revealed virus–host abundance (from DNA) and activity (from RNA) ratios consistently exceeding 1:1, suggesting a top‐heavy intra‐mat trophic structure with respect to virus–host interactions. Overall, our article contributes a curated database of viral sequences found in Caribbean coral reef benthic cyanobacterial mats (vMAT database) and provides multiple lines of field‐based evidence demonstrating that viruses are active members of mat communities, with broader implications for mat functional ecology and demography.

Viral association with cyanobacterial mat community mortality

“…Similar viral-induced collapses of low-evenness bloom events resulting from density-dependent viral predation (Thingstad, 2000) have been observed in other prokaryotic and eukaryotic algal blooms (Bratbak et al, 1993;Gons et al, 2002;Nagasaki et al, 1994). Viruses within BCMs on reefs around Bonaire were recently found to be naturally highly active members of mat communities (Cissell & McCoy, 2023). If and how cellular death from viral predation within mat-building populations scales to the mortality of entire mat communities or bloom events, however, remain unresolved, and the natural history of viruses in microbial mats more generally remains strikingly understudied (Cissell & McCoy, 2022b;Stal et al, 2019).…”

“…Many of the viruses recovered from this decaying mat were genetically similar to the metavirome of apparently healthy BCM communities at the same reef site (Appendix S1: Section S2, Figures S6 and S7; Cissell & McCoy, 2023). The VMR of the dominant cyanobacterial MAG in the Living sample was close to the natural diel variability of VMR associated with this other characterized BCM virome.…”

“…The VMR of the dominant cyanobacterial MAG in the Living sample was close to the natural diel variability of VMR associated with this other characterized BCM virome. In contrast, the VMRs in the Border and Decay samples were much higher than the natural diel variability in the linkage strengths of viral trophic interactions (Cissell & McCoy, 2023). Microbial populations and their viruses generally display markedly sustained patterns of coexistence (Kauffman et al, 2022).…”

“…Supplementary methods and supplementary results are presented in Appendix S1: Sections S1 and S2, respectively. Normalized abundances (from DNA read recruitment; copies per million [CPM]) of unique viral sequences recovered from this sequencing effort-a useful proxy for predicting viral dynamics in these samples (Cissell & McCoy, 2023)-were tracked across the transect. Abundance profiles overall suggested a potential increase in viral lytic activity in the Decay sample over the other samples from the transect, with a marked increase in the median and upper quartile of the abundance distribution in the Decay sample (Figure 2b; Appendix S1: Figure S2).…”

Divide and conquer: Spatial and temporal resource partitioning structures benthic cyanobacterial mats

“…Defense genes specifically targeting viruses and coevolution between viruses and specific bacteria have been observed in BCMs, showing potential key interactions between microbes in mats (Guajardo-Leiva et al, 2018;Wong et al, 2018). Viruses can influence mats via lysis, but these effects are density dependent wherein dynamics may favor lysogeny at high densities (Cissell & McCoy, 2023b, 2023c. Furthermore, selective lysing of microbial members may disrupt metabolically connected populations, affecting mat nutrient cycling and competitive and cooperative interactions, completely restructuring BCM communities.…”