Dianna L. Berry

Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics.

Harmful algal blooms (HABs) cause significant economic and ecological damage worldwide. Despite considerable efforts, a comprehensive understanding of the factors that promote these blooms has been lacking, because the biochemical pathways that facilitate their dominance relative to other phytoplankton within specific environments have not been identified. Here, biogeochemical measurements showed that the harmful alga Aureococcus anophagefferens outcompeted co-occurring phytoplankton in estuaries with elevated levels of dissolved organic matter and turbidity and low levels of dissolved inorganic nitrogen. We subsequently sequenced the genome of A. anophagefferens and compared its gene complement with those of six competing phytoplankton species identified through metaproteomics. Using an ecogenomic approach, we specifically focused on gene sets that may facilitate dominance within the environmental conditions present during blooms. A. anophagefferens possesses a larger genome (56 Mbp) and has more genes involved in light harvesting, organic carbon and nitrogen use, and encoding selenium- and metal-requiring enzymes than competing phytoplankton. Genes for the synthesis of microbial deterrents likely permit the proliferation of this species, with reduced mortality losses during blooms. Collectively, these findings suggest that anthropogenic activities resulting in elevated levels of turbidity, organic matter, and metals have opened a niche within coastal ecosystems that ideally suits the unique genetic capacity of A. anophagefferens and thus, has facilitated the proliferation of this and potentially other HABs.

Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation.

Cyanobacteria blooms caused by species such as Microcystis have become commonplace in many freshwater ecosystems. Although phosphorus (P) typically limits the growth of freshwater phytoplankton populations, little is known regarding the molecular response of Microcystis to variation in P concentrations and sources. For this study, we examined genes involved in P acquisition in Microcystis including two high-affinity phosphate-binding proteins (pstS and sphX) and a putative alkaline phosphatase (phoX). Sequence analyses among ten clones of Microcystis aeruginosa and one clone of Microcystis wesenbergii indicates that these genes are present and conserved within the species, but perhaps not the genus, as phoX was not identified in M. wesenbergii. Experiments with clones of M. aeruginosa indicated that expression of these three genes was strongly upregulated (50- to 400-fold) under low inorganic P conditions and that the expression of phoX was correlated with alkaline phosphatase activity (p < 0.005). In contrast, cultures grown exclusively on high levels of organic phosphorus sources (adenosine 5′-monophosphate, β-glycerol phosphate, and d-glucose-6-phosphate) or under nitrogen-limited conditions displayed neither high levels of gene expression nor alkaline phosphatase activity. Since Microcystis dominates phytoplankton assemblages in summer when levels of inorganic P (Pi) are often low and/or dominate lakes with low Pi and high organic P, our findings suggest this cyanobacterium may rely on pstS, sphX, and phoX to efficiently transport Pi and exploit organic sources of P to form blooms.

Shifts in Cyanobacterial Strain Dominance during the Onset of Harmful Algal Blooms in Florida Bay, USA

Cyanobacteria are fundamental components of aquatic phytoplankton communities and some taxa can cause harmful blooms in coastal ecosystems. Harmful cyanobacterial blooms are typically comprised of multiple strains of a single genus or species that cannot be resolved microscopically. Florida Bay, USA, has experienced harmful cyanobacterial blooms that have been associated with the loss of eelgrass, spiny lobsters, and general food web disruption for more than two decades. To identify the strain or strains of cyanobacteria forming blooms in Florida Bay, samples were collected across the system over an annual cycle and analyzed via DNA sequencing using cyanobacterial-specific 16S rRNA gene primers, flow cytometry, and scanning electron microscopy. Analyses demonstrated that the onset of blooms in Florida Bay was coincident with a transformation of the cyanobacterial populations. When blooms were absent, the cyanobacterial population in Florida Bay was dominated by phycoerythrin-containing Synechococcus cells that were most similar to strains within Clade III. As blooms developed, the cyanobacterial community transitioned to dominance by phycocyanin-containing Synechococcus cells that were coated with mucilage, chain-forming, and genetically most similar to the coastal strains within Clade VIII. Clade VIII strains of Synechococcus are known to grow rapidly, utilize organic nutrients, and resist top-down control by protozoan grazers and viruses, all characteristics consistent with observations of cyanobacterial blooms in Florida Bay. Further, the strains of Synechococcus blooming in this system are genetically distinct from the species previously thought to cause blooms in Florida Bay, Synechococcus elongatus. Collectively, this study identified the causative organism of harmful cyanobacterial blooms in Florida Bay, demonstrates the dynamic nature of cyanobacterial stains within genera in an estuary, and affirms factors promoting Synechococcus blooms.