Metatranscriptomics reveals gene expression dynamics during an anatoxin-a producing Dolichospermum bloom in a western coastal lake.

Abstract

Cyanobacteria harmful algal blooms in lakes are primarily driven by nutrient and temperature conditions, yet the interplay of these abiotic factors with microbial community dynamics during bloom events is complex and challenging to unravel. Despite advances through deep sequencing approaches, the underlying transcriptomic changes occurring within blooming and non-blooming taxa remains an actively expanding area of study. In this work, we examined a spring-summer bloom event in Anderson Lake, WA, which has experienced recurring annual blooms dominated by the filamentous, anatoxin-a producing, diazotroph: Dolichospermum sp. WA102. Our data reveal the overall transcriptional dominance by Dolichospermum sp. WA102 during the bloom, initiated with increasing temperature and light intensity under high available phosphorus but low nitrogen conditions. We find that heterocyst differentiation was already transcriptionally initiated prior to the bloom, facilitating downstream gene cascades necessary for rapid nitrogen fixation and metabolism. As the bloom progresses, phosphorus becomes depleted, necessitating the expression of Pho regulon components in Dolichospermum sp. WA102 and possibly curtailing the bloom itself. We dissect toxin production and the transcriptional subtleties of the anatoxin-a synthesis locus. Additionally, co-occurring taxa exhibited distinct gene expression profiles, with competition for nutrients, light, and potential allelopathic interactions acting as drivers. Overall, our data provide a unique transcriptomic perspective on a single-taxa-driven, anatoxin-producing bloom, highlighting its competitive adaptation to nutrient acquisition and favorable conditions. This deeper understanding of the genetic mechanisms underlying algal bloom events may aid in predicting and preventing future blooms.