Cyanobacterial Toxins of the Laurentian Great Lakes, Their Toxicological Effects, and Numerical Limits in Drinking Water

Abstract

Cyanobacteria are ubiquitous phototrophic bacteria that inhabit diverse environments across the planet. Seasonally, they dominate many eutrophic lakes impacted by excess nitrogen (N) and phosphorus (P) forming dense accumulations of biomass known as cyanobacterial harmful algal blooms or cyanoHABs. Their dominance in eutrophic lakes is attributed to a variety of unique adaptations including N and P concentrating mechanisms, N₂ fixation, colony formation that inhibits predation, vertical movement via gas vesicles, and the production of toxic or otherwise bioactive molecules. While some of these molecules have been explored for their medicinal benefits, others are potent toxins harmful to humans, animals, and other wildlife known as cyanotoxins. In humans these cyanotoxins affect various tissues, including the liver, central and peripheral nervous system, kidneys, and reproductive organs among others. They induce acute effects at low doses in the parts-per-billion range and some are tumor promoters linked to chronic diseases such as liver and colorectal cancer. The occurrence of cyanoHABs and cyanotoxins in lakes presents challenges for maintaining safe recreational aquatic environments and the production of potable drinking water. CyanoHABs are a growing problem in the North American (Laurentian) Great Lakes basin. This review summarizes information on the occurrence of cyanoHABs in the Great Lakes, toxicological effects of cyanotoxins, and appropriate numerical limits on cyanotoxins in finished drinking water.

Keywords: acetylcholinesterase; anatoxin-a; anatoxin-a(S); cyanobacteria; cylindrospermopsin; drinking water; microcystin; neurotoxicity; phosphatase inhibitor; saxitoxin.

Figure 1

Base structure of microcystins. R¹ and R² may be a methyl group or hydrogen. Dotted lines indicate peptide bonds.

Figure 2

Structure of cylindrospermopsin (R¹ = OH, R² = H), 7-epicylindrospermopsin (R¹ = H, R² = OH), and 7-deoxycylindrospermopsin (R¹ = H, R² = H).

Figure 3

Structure of anatoxin-a (R = H) and homoanatoxin-a (R = CH₃).

Figure 4

Structure of anatoxin-a(S).

Figure 5

Saxitoxin base structure. R¹, R², and R³ may be a combination of H, OH, or OSO₃⁻ and R⁴ may be one of OH, carbamoyl, or N-sulfo-carbamoyl groups.

Figure 6

Cyanobacterial floating scums in (A) Lake Winnebago, WI in August 2013, and (B) Lake Mendota, WI in September 2008, showing the bright blue appearance due to C-phycocyanin.

Figure 7

Average number of days surface water temperature above thresholds in the Great Lakes, 1992–2013. Data from National Oceanic and Atmospheric Administration, Great Lakes Environmental Research Laboratory, Great Lakes Sea Surface Environmental Analysis [1].

Figure 8

Concentrations (µg/L) of microcystins detected in a transect across Green Bay in August, 2014.

Figure 9

Distribution of total Phosphorus and microcystin across Lake Erie. Total P is the mean Spring concentration measured in 2008–2012. Microcystin data spans 2010–2015 from the Ohio EPA. No data is provided for Lake St. Clair north of Lake Erie.

Figure 10

Concentrations of MCs in finished and intake drinking water at Carroll County (top) and Toledo (bottom), OH plants in 2013 and 2014, respectively.

Figure 11

Dose-to-death curve for MCLR in the rat. Data from Hooser et al. 1989 [152].

Figure 12

Increase in organ and body weights due to oral exposure to 0–240 µg/kg·b.w. cylindrospermopsin. Data from Humpage and Falconer 2002.

Figure 13

Variability in drinking water ingestion rates across all age groups and percentiles (left) and resulting microcystin advisory levels for children under six calculated using drinking water ingestion rates (right). Note, the right x-axis is on a log scale. The middle black bar in each box represents the median, and the box width represents the upper and lower quartiles.

Figure 14

Variability in calculated cylindrospermopsin advisory levels at all age levels and drinking water ingestion rates using a NOAEL of 30 µg/kg.

Figure 15

Variability in calculated saxitoxin advisory levels at all age levels and drinking water ingestion rates using a NOAEL of 0.5 µg/kg.