Controlling harmful cyanobacterial blooms in a climatically more extreme world: management options and research needs

Cyanobacteria have a long evolutionary history that has been instrumental in allowing them to adapt to long-term geochemical and climatic changes, as well as current human and climatic alterations of aquatic ecosystems; e.g. nutrient over-enrichment, hydrologic modifications and warming. Harmful (toxic, hypoxia-generating, food web altering) cyanobacterial bloom (CyanoHAB) genera are particularly adept at taking advantage of these changes and perturbations. In addition, they have developed numerous mutualistic and symbiotic associations with other microbes and higher flora and fauna, and they modulate positive biogeochemical feedbacks, instrumental in their survival and dominance in diverse ecosystems. CyanoHABs are controlled by the combined and often synergistic effects of nutrient (nitrogen and phosphorus) inputs, light, temperature, water residence/flushing times, and biotic interactions. Accordingly, mitigation strategies are oriented towards manipulating these dynamic factors. Physical, chemical (nutrient) and biological manipulations can be effective in reducing CyanoHABs. However, these manipulations should also be accompanied by nutrient (both nitrogen and phosphorus in most cases) input reductions to ensure long-term success and sustainability. A major research and management goal for long-term control of CyanoHABs is to develop strategies that are adaptive to climatic variability and change, because nutrient-CyanoHAB thresholds are likely to be altered in a climatically more extreme world

Elevated organic carbon pulses persist in estuarine environment after major storm events

Estuaries regulate transport of dissolved organic carbon (DOC) from land to ocean. Export of terrestrial DOC from coastal watersheds is exacerbated by increasing major rainfall and storm events and human activities, leading to pulses of DOC that are shunted through rivers downstream to estuaries. Despite an upward trend of extreme events, the fate of the pulsed terrestrial DOC in estuaries remains unclear. We analyzed the effects of seven major tropical cyclones (TC) from 1999 to 2017 on the quantity and fate of DOC in the Neuse River Estuary (NC, USA). Significant TC-induced increases in DOC were observed throughout the estuary; the increase lasting from around 50 d at head-of-tide to over 6 months in lower estuary. Our results suggest that pulsed terrestrial DOC associated with TCs temporarily overwhelms the estuarine filter's abiotic and biotic degradation capacity under such high flow events, enhancing the shunt of terrestrial carbon to the coastal ocean.Non peer reviewe

Impacts of Seasonality and Nutrients on Microbial Mat Community Structure and Function

To understand the mechanisms responsible for seasonal fluctuations in growth and N2 fixation in intertidal microbial mat communities, we quantified seasonal changes in mat community composition, related these changes to diel and seasonal N2 fixation rates, and evaluated community responses (growth, N2fixation, composition) to long-term (22 d) nutrient addition bioassays. A temperate intertidal cyanobacterial mat community, located in coastal North Carolina, USA, was sampled at monthly intervals for 1 yr (1993-94) to determine changes in community composition. The abundances of major phototrophic groups were quantified based on the relative concentrations of taxaspecific photopigments (chlorophylls and carotenoids). The most abundant phototrophs were cyanobacteria, diatoms, and photosynthetic bacteria. Mat blomass and community composition underwent marked changes on both monthly and seasonal scales and corresponded with seasonal shifts in the diel patterns of N2 fixation. Diatom biomass increased during periods of low N2 fixation. Nutrient (nitrate and phosphate) addition bioassays indicated that both cyanobacterial and diatom growth were N limited. Cyanobacteria were able to circumvent N limitation by N2 fixation. The addition of high concentrations of N (100µM NaNO3) in combination with P (100 µM NaH2P04) resulted in an increase (163%) in the relative abundance of diatoms The addition of P alone more than doubled N2 fixation rates and cyanobacterial abundance increased (+34%) relative to diatoms. However, N and NP additions significantly lowered (by more than 75%) N2 fixation rates. Here we show that manipulative experiments, together with quantitative assessments of community composition based on chemotaxonomic pigments, can provide useful insights into the mechanisms that relate mat community structure and function to environmental constraints, including nutrient limitation and seasonal climatic changes

Moving towards adaptive management of cyanotoxin-impaired water bodies

The cyanobacteria are a phylum of bacteria that have played a key role in shaping the Earth's biosphere due to their pioneering ability to perform oxygenic photosynthesis. Throughout their history, cyanobacteria have experienced major biogeochemical changes accompanying Earth's geochemical evolution over the past 2.5+ billion years, including periods of extreme climatic change, hydrologic, nutrient and radiation stress. Today, they remain remarkably successful, exploiting human nutrient over-enrichment as nuisance "blooms." Cyanobacteria produce an array of unique metabolites, the functions and biotic ramifications of which are the subject of diverse ecophysiological studies. These metabolites are relevant from organismal and ecosystem function perspectives because some can be toxic and fatal to diverse biota, including zooplankton and fish consumers of algal biomass, and high-level consumers of aquatic food sources and drinking water, including humans. Given the long history of environmental extremes and selection pressures that cyanobacteria have experienced, it is likely that that these toxins serve ecophysiological functions aimed at optimizing growth and fitness during periods of environmental stress. Here, we explore the molecular and ecophysiological mechanisms underlying cyanotoxin production, with emphasis on key environmental conditions potentially controlling toxin production. Based on this information, we offer potential management strategies for reducing cyanotoxin potentials in natural waters; for cyanotoxins with no clear drivers yet elucidated, we highlight the data gaps and research questions that are still lacking. We focus on the four major classes of toxins (anatoxins, cylindrospermopsins, microcystins and saxitoxins) that have thus far been identified as relevant from environmental health perspectives, but caution there may be other harmful metabolites waiting to be elucidated

Fish Kills and Bottom-Water Hypoxia in the Neuse River and Estuary: Reply to Burkholder et al.

Burkholder et al. (1999) authored a comment in Manne Ecology Progress Series (MEPS) that selectively criticizes elements of our findings that appeared earlier in the same journal (Paerl et al. 1998). For the benefit of the readership of MEPS, it would have been useful to have had both their comment and our reply in the same volume. Unfortunately, we were not informed of their comment pnor to its publication

Molecular insights into a dinoflagellate bloom

In coastal waters worldwide, an increase in frequency and intensity of algal blooms has been attributed to eutrophication, with further increases predicted because of climate change. Yet, the cellular-level changes that occur in blooming algae remain largely unknown. Comparative metatranscriptomics was used to investigate the underlying molecular mechanisms associated with a dinoflagellate bloom in a eutrophied estuary. Here we show that under bloom conditions, there is increased expression of metabolic pathways indicative of rapidly growing cells, including energy production, carbon metabolism, transporters and synthesis of cellular membrane components. In addition, there is a prominence of highly expressed genes involved in the synthesis of membrane-associated molecules, including those for the production of glycosaminoglycans (GAGs), which may serve roles in nutrient acquisition and/or cell surface adhesion. Biotin and thiamine synthesis genes also increased expression along with several cobalamin biosynthesis-associated genes, suggesting processing of B12 intermediates by dinoflagellates. The patterns in gene expression observed are consistent with bloom-forming dinoflagellates eliciting a cellular response to elevated nutrient demands and to promote interactions with their surrounding bacterial consortia, possibly in an effort to cultivate for enhancement of vitamin and nutrient exchanges and/or direct consumption. Our findings provide potential molecular targets for bloom characterization and management efforts

Extreme Weather Events and Climate Variability Provide a Lens to How Shallow Lakes May Respond to Climate Change

Shallow lakes, particularly those in low-lying areas of the subtropics, are highly vulnerable to changes in climate associated with global warming. Many of these lakes are in tropical cyclone strike zones and they experience high inter-seasonal and inter-annual variation in rainfall and runoff. Both of those factors strongly modulate sediment–water column interactions, which play a critical role in shallow lake nutrient cycling, water column irradiance characteristics and cyanobacterial harmful algal bloom (CyanoHAB) dynamics. We illustrate this with three examples, using long-term (15–25 years) datasets on water quality and plankton from three shallow lakes: Lakes Okeechobee and George (Florida, USA) and Lake Taihu (China). Okeechobee and Taihu have been impacted repeatedly by tropical cyclones that have resulted in large amounts of runoff and sediment resuspension, and resultant increases in dissolved nutrients in the water column. In both cases, when turbidity declined, major blooms of the toxic CyanoHAB Microcystis aeruginosa occurred over large areas of the lakes. In Lake George, periods of high rainfall resulted in high dissolved color, reduced irradiance, and increased water turnover rates which suppress blooms, whereas in dry periods with lower water color and water turnover rates there were dense cyanobacteria blooms. We identify a suite of factors which, from our experience, will determine how a particular shallow lake will respond to a future with global warming, flashier rainfall, prolonged droughts and stronger tropical cyclones

Ecosystem Responses to Internal and Watershed Organic Matter Loading: Consequences for Hypoxia in the Eutrophying Neuse River Estuary, North Carolina, USA

The contrasting impacts of externally supplied (runoff) and internally generated (nutrient stimulated phytoplankton blooms) organic matter on oxygen (02) depletion were examined and evaluated in the eutrophic, salinity-stratified Neuse River Estuary, North Carolina, USA. This nitrogen (N)- limited estuary is experiencing increasing anthropogenic N loading from expanding urban, agricultural and industrial development in its watershed. Resultant algal blooms, which provided organic matter loads capable of causing extensive low 02 (hypoxic) and depleted 02 (anoxic) conditions, have induced widespread mortality of resident fin- and shellfish. Phytoplankton blooms followed periods of elevated N loading, except during extremely high runoff periods (e.g. hurricanes), when high rates of flushing and reduced water residence times did not allow sufficient time for bloom development. During these periods, hypoxia and anoxia were dominated by watershed-derived organic matter loading. Externally vs internally generated organic matter loading scenarios were examined in sequential years (1994 to 1996) to compare the differential impacts of an average discharge year (l0 yr mean hydrological conditions) (1994), N-stimulated summer algal blooms [1995), and a major hurricane (Fran; September 1996). The responses of primary production, hypoxia, and anoxia to these hydrologically contrasting years and resultant organic matter loadings help distinguish watershed from internal forcing of 02 dynamics and fish kills

Watershed-Scale Drivers of Air-Water CO2 Exchanges in Two Lagoonal North Carolina (USA) Estuaries

Riverine loading of nutrients and organic matter act in concert to modulate CO2 fluxes in estuaries, yet quantitative relationships between these factors remain poorly defined. This study explored watershed-scale mechanisms responsible for the relatively low CO2 fluxes observed in two microtidal, lagoonal estuaries. Air-water CO2 fluxes were quantified with 74 high-resolution spatial surveys in the neighboring New River Estuary (NewRE) and Neuse River Estuary (NeuseRE), North Carolina, which experience a common climatology but differ in marine versus riverine influence. Annually, both estuaries were relatively small sources of CO2 to the atmosphere, 12.5 and 16.3mmolCm(-2)d(-1) in the NeuseRE and NewRE, respectively. Large-scale pCO(2) variations were driven by changes in freshwater age, which modulates nutrient and organic carbon supply and phytoplankton flushing. Greatest pCO(2) undersaturation was observed at intermediate freshwater ages, between 2 and 3weeks. Biological controls on CO2 fluxes were obscured by variable inputs of river-borne CO2, which drove CO2 degassing in the river-dominated NeuseRE. Internally produced CO2 exceeded river-borne CO2 in the marine-dominated NewRE, suggesting that net ecosystem heterotrophy, rather than riverine inputs, drove CO2 fluxes in this system. Variations in riverine alkalinity and inorganic carbon loading caused zones of minimum buffering capacity to occur at different locations in each estuary, enhancing the sensitivity of estuarine inorganic C chemistry to acidification. Although annual CO2 fluxes were similar between systems, watershed-specific hydrologic factors led to disparate controls on internal carbonate chemistry, which can influence ecosystem biogeochemical cycling, trophic state, and response to future perturbations. Plain Language Summary Estuaries release nearly as much CO2 to the atmosphere as is taken up over the continental shelf. However, estuarine emissions vary greatly across space and time, contributing significantly to the uncertainty of global carbon budgets. In this study, we assess spatial and temporal variability in CO2 emissions from adjacent estuaries in North Carolina, USA. These emissions varied across seasons and river discharge conditions but were relatively small when assessed as annual averages. Freshwater age (time freshwater spends in estuary before being flushed to ocean) was an important driver of CO2 dynamics in both estuaries, due to its role in regulating nutrient, DOC, and DIC supply while also affecting the rate at which phytoplankton are flushed from the system. While the relationship between freshwater age and CO2 was similar for both estuaries, we show that the various external and internal inputs of CO2 were quite different. Riverine CO2 inputs drove CO2 emissions in the river-dominated estuary, while internally produced CO2 (from community respiration) was more important in the marine-dominated estuary. We also demonstrate that poorly buffered regions in both estuaries are particularly vulnerable to acidification, with potentially negative impacts on calcifying organisms