Shotgun metagenomic sequencing reveals the full taxonomic, trophic, and functional diversity of a coral reef benthic cyanobacterial mat from Bonaire, Caribbean Netherlands

Abstract

Anthropogenic forcing is spurring cyanobacterial proliferation in aquatic ecosystems worldwide. While planktonic cyanobacterial blooms have received substantial research attention, benthic blooms of mat-forming cyanobacteria have received considerably less attention, especially benthic mat blooms on coral reefs. Resultingly, numerous aspects of coral reef benthic cyanobacterial bloom ecology remain unknown, including underlying biodiversity in the mat communities. Most previous characterizations of coral reef cyanobacterial mat composition have only considered the cyanobacterial component. Without an unbiased characterization of full community diversity, we cannot predict whole-community response to anthropogenic inputs or effectively determine appropriate mitigation strategies. Here, we advocate for the implementation of shotgun sequencing techniques to study coral reef cyanobacterial mats worldwide, utilizing a case study of a coral reef benthic cyanobacterial mat sampled from the island of Bonaire, Caribbean Netherlands. Read-based taxonomic profiling revealed that Cyanobacteria was present at only 47.57% relative abundance in a coral reef cyanobacterial mat, with non-cyanobacterial members of the sampled mat community, including diatoms (0.78%), fungi (0.25%), Archaea (0.34%), viruses (0.08%), and other bacteria (45.78%), co-dominating the community. We found numerous gene families for regulatory systems and for functional pathways (both aerobic and anaerobic). These gene families were involved in community coordination; photosynthesis; nutrient scavenging; and the cycling of sulfur, nitrogen, phosphorous, and iron. We also report bacteriophage (including prophage) sequences associated with this subtidal coral reef cyanobacterial mat, which could contribute to intra-mat nutrient cycling and bloom dynamics. Overall, our results suggest that Cyanobacteria-focused analysis of coral reef cyanobacterial mats underestimates mat diversity and fails to capture community members possessing broad metabolic potential for intra-mat nutrient scavenging, recycling, and retention that likely contribute to the contemporary success of cyanobacterial mats on reefs. We advocate for increased collaboration between microbiologists and coral reef ecologists to unite insights from each discipline and improve efforts to understand mat ecology.