Abstract

While harmful algal blooms caused by the ichthyotoxic dinoflagellate, Cochlodinium (Margalefidinium) polykrikoides, are allelopathic and may have unique associations with bacteria, a comprehensive assessment of the planktonic communities associated with these blooms has been lacking. Here, we used high-throughput amplicon sequencing to assess size fractionated (0.2 and 5 μm) bacterial (16S) and phytoplankton assemblages (18S) associated with blooms of C. polykrikoides during recurrent blooms in NY, USA. Over a three-year period, samples were collected inside (‘patch’) and outside (‘non-patch’) dense accumulations of C. polykrikoides to assess the microbiome associated with these blooms. Eukaryotic plankton communities of blooms had significantly lower diversity than non-bloom samples, and non-bloom samples hosted 30 eukaryotic operational taxonomic units (OTUs) not found within blooms, suggesting they may have been allelopathically excluded from blooms. Differential abundance analyses revealed that C. polykrikoides blooms were significantly enriched in dinoflagellates (p<0.001) and the experimental enrichment of C. polykrikoides led to a significant increase in the relative abundance of eight genera of dinoflagellates but a significant decline in other eukaryotic plankton. Amoebophrya co-dominated both within- and near- C. polykrikoides blooms and was more abundant in bloom patches. The core bacterial microbiome of the >0.2μm fraction of blooms was dominated by an uncultured bacterium from the SAR11 clade, while the >5μm size fraction was co-dominated by an uncultured bacterium from Rhodobacteraceae and Coraliomargarita. Two bacterial lineages within the >0.2μm fraction, as well as the Gammaproteobacterium, Halioglobus, from the >5μm fraction were unique to the microbiome of blooms, while there were 154 bacterial OTUs only found in non-bloom waters. Collectively, these findings reveal the unique composition and potential function of eukaryotic and prokaryotic communities associated with C. polykrikoides blooms.

Highlights

  • While differential abundance analyses revealed that Dinophyceae was significantly (p

  • This study identified the microbial consortium associated with C. polykrikoides blooms and revealed that C. polykrikoides blooms were enriched in dinoflagellates and depleted in diatoms (>5μm fraction) among eukaryotes, and enriched in Rhodobacteraceae and depleted in Flavobacteriaceae, Rhodospirillaceae and the SAR11 clade among prokaryotes

  • Amoebophrya was highly abundant both within and near blooms while lineages of Geminigera sp., Cylindrotheca closterium, Leptocylindrus spp., an uncultured eukaryote from MAST-3J, and Pirsonia sp., were unique members of the core eukaryotic microbiomes found inside blooms

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Summary

Introduction

Over the past three decades, blooms have expanded to other regions along the US east coast, including the York River and Chesapeake Bay, Virginia [4,5], Skidaway Estuary, Georgia [6], Indian River Lagoon, Florida [7], multiple embayments across Long Island, New York [2,8,9,10,11], and Cape Cod, Massachusetts [12] This ichthyotoxic dinoflagellate is well-known for causing fish kills across North America and Asia [1,2,13,14], causing significant financial losses (up to $100M) during bloom events [15,16,17]. There remains great interest in determining what causes these destructive blooms to recur and expand on a global scale

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