High-Resolution Spatiotemporal Dynamics of Harmful Algae in the Indian River Lagoon (Florida)—A Case Study of Aureoumbra lagunensis, Pyrodinium bahamense, and Pseudo-nitzschia

The Indian River Lagoon (IRL), located on the east coast of Florida, is a complex estuarine ecosystem that is negatively affected by recurring harmful algal blooms (HABs) from distinct taxonomic/functional groups. Enhanced monitoring was established to facilitate rapid quantification of three recurrent bloom taxa, Aureoumbra lagunensis, Pyrodinium bahamense, and Pseudo-nitzschia spp., and included corroborating techniques to improve the identification of small-celled nanoplankton (<10 μm in diameter). Identification and enumeration of these target taxa were conducted during 2015–2020 using a combination of light microscopy and species-specific approaches, specifically immunofluorescence flow cytometry as well as a newly developed qPCR assay for A. lagunensis presented here for the first time. An annual bloom index (ABI) was established for each taxon based on occurrence and abundance data. Blooms of A. lagunensis (>2 × 108 cells L–1) were observed in all 6 years sampled and across multiple seasons. In contrast, abundance of P. bahamense, largely driven by the annual temperature cycle that moderates life cycle transitions and growth, displayed a strong seasonal pattern with blooms (105–107 cells L–1) generally developing in early summer and subsiding in autumn. However, P. bahamense bloom development was delayed and abundance was significantly lower in years and locations with sustained A. lagunensis blooms. Pseudo-nitzschia spp. were broadly distributed with sporadic bloom concentrations (reaching 107 cells L–1), but with minimal concentrations of the toxin domoic acid detected (<0.02 μg L–1). In summer 2020, multiple monitoring tools characterized a novel nano-cyanobacterium bloom (reaching 109 cells L–1) that coincided with a decline in A. lagunensis and persisted into autumn. Statistical and time-series analyses of this spatiotemporally intensive dataset highlight prominent patterns in variability for some taxa, but also identify challenges of characterizing mechanisms underlying more episodic yet persistent events. Nevertheless, the intersect of temperature and salinity as environmental proxies proved to be informative in delineating niche partitioning, not only in the case of taxa with long-standing data sets but also for seemingly unprecedented blooms of novel nanoplanktonic taxa.

Bivalve Feeding on the Brown Tide Aureoumbra lagunensis in a Shallow Coastal Environment

Brown tides formed by Aureoumbra lagunensis decrease light penetration in the water column and are often followed by hypoxic events that result in the loss of fish and shellfish. To understand the ability of bivalve filter feeders to control and prevent A. lagunensis blooms, we exposed eastern oysters (Crassostrea virginica), hooked mussels (Ischadium recurvum), and hard clams (Mercenaria mercenaria) to a naturally co-occurring brown tide in the Indian River Lagoon (IRL), Florida, United States. Bivalves were exposed in the laboratory to multiple concentrations (104 to 106 cells mL–1) of isotopically labeled (13C and 15N) A. lagunensis cells. The standard clearance rate (herein clearance rate) of each bivalve species was calculated using flow cytometry to quantify A. lagunensis cell removal. The highest clearance rates were at 104 cells mL–1, but values varied across bivalve species (2.16 ± 0.30, 3.03 ± 0.58, and 0.41 ± 0.12 L h–1 for C. virginica, I. recurvum, and M. mercenaria, respectively). Although clearance rates decreased with increasing bloom concentrations, bivalves were still consuming algal cells at all concentrations and were retaining and assimilating more cells at the highest concentrations, as revealed by δ13C and δ15N values. We highlight interspecific differences among bivalve species in the removal of A. lagunensis, supporting the importance of healthy and diverse filter feeding communities in estuaries, especially as threats of brown tides and other HABs are increasing in the Anthropocene.

Transcriptomic Responses of Four Pelagophytes to Nutrient (N, P) and Light Stress

Pelagophytes are abundant picophytoplankton within open ocean ecosystems and the causative algae of harmful brown tide blooms in estuaries. The physiological capabilities facilitating the ecological success of pelagophytes in these diverse ecosystems remains poorly understood. Here, we investigated the transcriptional response of two coastal pelagophytes (Aureococcus anophagefferens and Aureoumbra lagunensis) and two open ocean pelagophytes (Pelagococcus subviridis and Pelagomonas calceolata) to conditions commonly found within the marine ecosystems where they thrive: low concentrations of nitrogen (N), phosphorus (P), or light. OrthoMCL was used to generate a total of 62,653 orthologous groups (OGs) with only a small fraction of these OGs (2,776 or 4.4%) being shared among all four pelagophytes. Of the commonly shared OGs, 8% were significantly differentially abundant under low N, P, or light with the majority associated with energy and lipid metabolism. Distinct responses among pelagophytes included increased abundance of transcripts encoding phosphate transporters (Aureococcus) and transcripts encoding a pyrophosphatase (Aureococcus and Pelagomonas) under low P, the expression of a suite of organic nitrogen-degrading enzymes under low N (Aureoumbra and Pelagomonas), increased abundance of transcripts encoding flavodoxins relative to ferredoxins (Pelagomonas) and transcripts encoding lysophospholipase (Pelagococcus) under low light, and both increases and decreases in abundance of transcripts encoding selenoproteins in all pelagophytes except Pelagococcus. Collectively, this study provides new information on the expressed gene compliment of these poorly characterized taxa and demonstrates that these pelagophytes possess a combination of shared and unique physiological features that likely facilitate their adaptation to distinct environmental conditions.

Mitochondrial genome evolution in pelagophyte algae

The Pelagophyceae are marine stramenopile algae that include Aureoumbra lagunensis and Aureococcus anophagefferens, two microbial species notorious for causing harmful algal blooms. Despite their ecological significance, relatively few genomic studies of pelagophytes have been carried out. To improve understanding of the biology and evolution of pelagophyte algae, we sequenced complete mitochondrial genomes for A. lagunensis (CCMP1510), Pelagomonas calceolata (CCMP1756) and five strains of A. anophagefferens (CCMP1707, CCMP1708, CCMP1850, CCMP1984 and CCMP3368) using Nanopore long-read sequencing. All pelagophyte mitochondrial genomes assembled into single, circular mapping contigs between 39,376 base-pairs (bp) (P. calceolata) and 55,968 bp (A. lagunensis) in size. Mitochondrial genomes for the five A. anophagefferens strains varied slightly in length (42,401 bp—42,621 bp) and were 99.4%-100.0% identical. Gene content and order was highly conserved between the A. anophagefferens and P. calceolata genomes, with the only major difference being a unique region in A. anophagefferens containing DNA adenine and cytosine methyltransferase (dam/dcm) genes that appear to be the product of lateral gene transfer from a prokaryotic or viral donor. While the A. lagunensis mitochondrial genome shares seven distinct syntenic blocks with the other pelagophyte genomes, it has a tandem repeat expansion comprising ∼40% of its length, and lacks identifiable rps19 and glycine tRNA genes. Laterally acquired self-splicing introns were also found in the 23S rRNA (rnl) gene of P. calceolata and the coxI gene of the five A. anophagefferens genomes. Overall, these data provide baseline knowledge about the genetic diversity of bloom-forming pelagophytes relative to non-bloom-forming species.

Spatial and temporal shifts in the diet of the barnacle Amphibalanus eburneus within a subtropical estuary

The success of many sessile invertebrates in marine benthic communities is linked to their ability to efficiently remove suspended organic matter from the surrounding water column. To investigate the diet of the barnacle Amphibalanus eburneus, a dominant suspension feeder within the Indian River Lagoon (IRL) of central Florida, we compared the stable isotopes ratios (δ13C and δ15N) of barnacle tissue to those of particulate organic matter (POM). Collections were carried out quarterly for a year from 29 permanent sites and at sites impacted by an Aureoumbra lagunensis bloom. δ13C and δ15N values of Amphibalanus eburneus varied across sites, but δ15N was more stable over time. There was a range of δ15N values of Amphibalanus eburneus tissue from 6.0‰ to 10.5‰ across sites. Because land-based sources such as sewage are generally enriched in 15N, this suggests a continuum of anthropogenic influence across sites in the IRL. Over 70% of the variation in δ15N values of Amphibalanus eburneus across sites was driven by the δ15N values of POM, supporting a generalist feeding strategy on available sources of suspended organic matter. The dominance of this generalist consumer in the IRL may be linked to its ability to consume spatially and temporally variable food resources derived from natural and anthropogenic sources, as well as Aureoumbra lagunensis cells. Generalist consumers such as Amphibalanus eburneus serve an important ecological role in this ecosystem and act as a sentinel species and recorder of local, site-specific isotopic baselines.