Cryptic bacterial pathogens of diatoms peak during senescence of a winter diatom bloom

Abstract

Diatoms are globally abundant algae that form extensive blooms in aquatic ecosystems. Certain bacteria behave antagonistically towards diatoms, killing or inhibiting their growth. Despite their crucial implications to diatom health and bloom control, insight of the prevalence and dynamics of antagonistic bacteria in nature is lacking. We report an ecosystem assessment of the diversity and seasonal patterns of bacterial antagonists of diatoms via regular plaque-assay sampling in the Western English Channel (WEC), where diatoms frequently bloom. Unexpectedly, peaks in antagonist detection did not occur during characteristic spring blooms, but coincided with a winter bloom of Coscinodiscus, suggesting bacterial pathogens likely influence distinct diatom host populations. We isolated multiple antagonists, spanning 4 classes and 10 bacterial orders. Many species had no prior reports of pathogenicity towards diatoms, and we verified diatom growth inhibitory effects of 8 isolates. In all cases tested, pathogenicity was activated by pre-exposure to diatom organic matter. Discovery of widespread cryptic antagonistic activity evident under specific conditions, indicates that bacterial pathogenicity towards diatoms is more prevalent than previously recognised. Finally, mining Tara Oceans data revealed the global biogeography of WEC antagonists and co-occurrence patterns with diatom hosts. Our study indicates that multiple, diverse antagonistic bacteria have potential to impact diatom growth and bloom dynamics in marine waters globally.

Seasonal niche overlap of diverse facultative antagonistic bacteria of diatoms in a productive coastal ecosystem

“…To assess the abundance and seasonal trends of bacterial antagonists, separate 16S BLAST databases were created using a non-rarified 16S amplicon dataset in Geneious Prime (Geneious Prime 2023.0.1, https://www.geneious.com). Full-length 16S rRNA gene sequences (Dataset S1) (Sohn et al 1978;Wang et al 2016;Van Tol, Amin and Armbrust 2017;Branscombe et al 2024) were queried against the 16S ASV database, and ASVs with a percentage pairwise identity above 97% (query cover 100%) were collated. Taxonomic assignment of each ASV was subsequently validated by constructing Maximum Likelihood trees.…”

“…The copyright holder for this preprint this version posted June 6, 2024. ; https://doi.org/10.1101/2024.06.05.594869 doi: bioRxiv preprint confer robust growth inhibitory effects against diatoms in laboratory culture (Branscombe et al 2024). We queried the 16S rRNA gene sequences of P. alexandrii, T. lohafexi, M. spongiicola, H. titanicae, M. adhaerens, M. idriensis, and V. diazotrophicus (Dataset S1).…”

“…Our recent work employing plaque-assay sampling to isolate a library of antagonistic bacteria of diatoms from L4 Station in the Western English Channel (WEC) identified multiple bacteria capable of causing severe detrimental effects on diatom growth (Branscombe et al 2024). Laboratory characterisation of eight of these strains revealed that in all cases, these effects were facultative, activated by pre-exposure to diatom necromass.…”

“…Moreover, detection of metabarcodes phylogenetically similar to several bacterial antagonists isolated from the WEC in marine ecosystems globally (Branscombe et al 2024), indicates the broader biogeography of such bacteria.…”

“…The close proximity of L4 Station off the coast of Plymouth lends itself to frequent sampling of diatom and bacterial assemblages (Gilbert et al 2009;Caporaso et al 2012;Taylor et al 2014;Taylor and Cunliffe 2016) and is underpinned by extensive long-term metadata of phytoplankton diversity and physicochemical parameters (McEvoy et al 2023). Exploiting these attributes combined with our previous knowledge gained from isolating facultative antagonistic bacteria from this region (Branscombe et al 2024), we aimed to assess the presence of such bacteria (as well as additional algicidal bacteria reported in the literature) to study their co-occurrence with phytoplankton in this productive coastal ecosystem where diatoms frequently bloom, using 16S and 18S metabarcoding.…”