Emerging harmful algal blooms caused by distinct seasonal assemblages of the toxic diatom Pseudo-nitzschia in Narragansett Bay, RI, USA

Abstract

The diatom Pseudo-nitzschia produces the neurotoxin domoic acid (DA) that bioaccumulates in shellfish, causing illness in humans and marine animals upon ingestion. In 2017, high levels of DA in shellfish meat closed shellfish harvest in Narragansett Bay (NBay), Rhode Island for the first time in history, although abundant Pseudo-nitzschia have been observed for over 50 years. What caused these events is unknown: whether an environmental factor altered endemic Pseudo-nitzschia physiology or new DA-producing strain(s) were introduced. To investigate, we conducted weekly sampling from 2017-2019 to compare with 2016 precautionary closure and 2017 closure samples. Particulate DA was quantified by highly sensitive LC-MS/MS and correlated with environmental metadata. Pseudo-nitzschia were identified using high-throughput rDNA sequencing, yielding a detailed understanding of distinct seasonal multi-species assemblages. Low DA was detected throughout 2017-2019, except in recurring peaks in the fall and early summer. Fall DA peaks contained toxigenic species (P. pungens var. pungens, P. multiseries, P. calliantha, and P. subpacifica) as well as a novel P. americana taxon. Fewer species were present during summer DA peaks including toxigenic P. multiseries, P. plurisecta, and P. delicatissima. Most 2017 closure samples contained P. australis. Our data showed P. australis as infrequent but particularly concerning. Recurring Pseudo-nitzschia assemblages were driven by seasonal temperature changes and DA correlated with low dissolved inorganic nitrogen. Thus, the NBay closures were likely caused by resident assemblages dependent on nutrient status as well as the episodic introductions of species that may be a result of oceanographic and climactic shifts.