Genetic variation of the bloom-forming Cyanobacterium Microcystis aeruginosa within and among lakes: implications for harmful algal blooms

Abstract

To measure genetic variation within and among populations of the bloom-forming cyanobacterium Microcystis aeruginosa, we surveyed a suite of lakes in the southern peninsula of Michigan that vary in productivity (total phosphorus concentrations of approximately 10 to 100 microg liter(-1)). Survival of M. aeruginosa isolates from lakes was relatively low (i.e., mean of 7% and maximum of 30%) and positively related to lake total phosphorus concentration (P = 0.014, r2 = 0.407, n = 14). In another study (D. F. Raikow, O. Sarnelle, A. E. Wilson, and S. K. Hamilton, Limnol. Oceanogr. 49:482-487, 2004), survival rates of M. aeruginosa isolates collected from an oligotrophic lake (total phosphorus of approximately 10 mug liter(-1) and dissolved inorganic nitrogen:total phosphorus ratio of 12.75) differed among five different medium types (G test, P of <0.001), with higher survival (P = 0.003) in low-nutrient media (28 to 37% survival) than in high-nutrient media. Even with the relatively low isolate survivorship that could select against detecting the full range of genetic variation, populations of M. aeruginosa were genetically diverse within and among lakes (by analysis of molecular variance, Phi(sc) = 0.412 [Phi(sc) is an F-statistic derivative which evaluates the correlation of haplotypic diversity within populations relative to the haplotypic diversity among all sampled populations], P = 0.001), with most clones being distantly related to clones collected from lakes directly attached to Lake Michigan (a Laurentian Great Lake) and culture collection strains collected from Canada, Scotland, and South Africa. Ninety-one percent of the 53 genetically unique M. aeruginosa clones contained the microcystin toxin gene (mcyA). Genotypes with the toxin gene were found in all lakes, while four lakes harbored both genotypes possessing and genotypes lacking the toxin gene.

FIG. 1.

Relationship between lake trophic status (measured as total phosphorus concentration [μg liter⁻¹]) and log (% isolate survival + 0.01) (% = no. of survivors/no. of total isolates collected).

FIG. 2.

Example of PCR gel of HIP products. HIP-CT and HIP-CA samples for M. aeruginosa isolates from Clark Lake (lanes 2 to 10), Gilkey Lake (lane 11), Gull Lake (lane 12), Hudson Lake (lanes 13 to 15), Magician Lake (lanes 16 to 17), PCC 7806 (lane 19, HIP-CT; lane 20, HIP-CA), and standards (lanes 1 and 20, HIP-CT; lanes 1 and 19, HIP-CA). Note differences among Clark Lake and Hudson Lake strains.

FIG. 3.

Phylogenetic tree for M. aeruginosa isolates created by calculating the relative “distances” of PCR products in a pairwise fashion between the banding patterns of each HIP-PCR (BANDAID program created by Tim Salmon and Brett Neilan at the University of New South Wales [50]). Toxin gene absence denoted by “lacks mcyA” in parentheses following strain name. All other strains contain the toxin gene. Scale = 1 relative distance unit.