Cryptic Diversity of Black Band Disease Cyanobacteria in Siderastrea siderea Corals Revealed by Chemical Ecology and Comparative Genome-Resolved Metagenomics

Abstract

Black band disease is a globally distributed and easily recognizable coral disease. Despite years of study, the etiology of this coral disease, which impacts dozens of stony coral species, is not completely understood. Although black band disease mats are predominantly composed of the cyanobacterial species Roseofilum reptotaenium, other filamentous cyanobacterial strains and bacterial heterotrophs are readily detected. Through chemical ecology and metagenomic sequencing, we uncovered cryptic strains of Roseofilum species from Siderastrea siderea corals that differ from those on other corals in the Caribbean and Pacific. Isolation of metabolites from Siderastrea-derived Roseofilum revealed the prevalence of unique forms of looekeyolides, distinct from previously characterized Roseofilum reptotaenium strains. In addition, comparative genomics of Roseofilum strains showed that only Siderastrea-based Roseofilum strains have the genetic capacity to produce lasso peptides, a family of compounds with diverse biological activity. All nine Roseofilum strains examined here shared the genetic capacity to produce looekeyolides and malyngamides, suggesting these compounds support the ecology of this genus. Similar biosynthetic gene clusters are not found in other cyanobacterial genera associated with black band disease, which may suggest that looekeyolides and malyngamides contribute to disease etiology through yet unknown mechanisms.

Novel diversity within Roseofilum (Desertifilaceae, Cyanobacteria) from marine benthic mats with description of four new species

“…This is also the first clear demarcation between BBD‐associated Roseofilum and non‐BBD‐associated species. With recent research indicating that BBD‐associated Roseofilum possess several biosynthetic gene clusters not found in other BBD‐associated cyanobacteria (Meyer et al, 2023), there is a need to evaluate the chemical and genetic diversity of Roseofilum from BBD‐associated and non‐BBD‐associated mats to shed more light into mechanisms of infection for BBD.…”

“…However, metagenomic sequencing work has captured Roseofilum in different environments across the globe (based on NCBI sequences), such as Pelorus Island (Australia), Miyako Island (Japan), Carrie Bow Cay (Belize), Luminao Reef Flat (Guam, United States), and Ft. Lauderdale (United States; Figure 1; Arotsker et al, 2009; Barneah et al, 2007; Buerger et al, 2016; Casamatta et al, 2012; Cooney et al, 2002; Frias‐Lopez et al, 2002; Hutabarat et al, 2018; Klaus et al, 2011; Meyer et al, 2016; Rasoulouniriana et al, 2009; Sato et al, 2010). Although the geographic distribution and chemical diversity of Roseofilum have been studied (Gunasekera et al, 2019; Meyer et al, 2023), there remains a lack of effort to elucidate species in the genus using a combination of morphological, molecular, and genomic data.…”

GINSA: an accumulator for paired locality and next-generation small ribosomal subunit sequence data

“…For instance, evolutionary biologists rely on large molecular sequence datasets to study speciation trends ( Schlegel 1991 , Adl et al 2019 ). Large datasets help resolve cryptic diversity, which is a challenge seen across the tree of life—animals ( Marchán et al 2018 , Li and Wiens 2023 ), plants ( Vieu et al 2023 , Windham et al 2023 ), fungi ( Koufopanou et al 1997 , Pringle et al 2005 ), bacteria ( Meyer et al 2023 ), protists ( Wakeman and Leander 2013 , Krienitz et al 2015 , Martin et al 2016 ), archaea ( Câmara et al 2023 ), and viruses ( Roux et al 2019 ). Specialists across a range of taxa can therefore use GINSA to collect more data for their phylogenetic (SSU sequence) and biogeographic (locality) analyses.…”

Freshwater Cyanobacterial Toxins, Cyanopeptides and Neurodegenerative Diseases

“…Outcompeting of symbiotic microorganisms may lead to disease development (examples: (1) Black Band disease of corals associated with cyclic peptides production by Roseophilum sp. cyanobacteria [ 350 ]; (2) association of the gut dysbiosis and ND such as Parkinson’s and Alzheimer’s diseases [ 351 , 352 ]). The mitochondria (likely evolved from prokaryotic endosymbionts) and cells that are high-energy demanding, such as neurons and cardiomyocytes, are likely to be affected by NCAA (example: BMAA induce mitochondrial dysfunction in neurons with cardiolipin exposure [ 353 , 354 ] and in embryonic cardiomyocytes leading to cardiac developmental defects [ 355 ].…”