Elevated pH Conditions Associated With Microcystis spp. Blooms Decrease Viability of the Cultured Diatom Fragilaria crotonensis and Natural Diatoms in Lake Erie

Abstract

Cyanobacterial Harmful Algal Blooms (CyanoHABs) commonly increase water column pH to alkaline levels ≥9.2, and to as high as 11. This elevated pH has been suggested to confer a competitive advantage to cyanobacteria such as Microcystis aeruginosa. Yet, there is limited information regarding the restrictive effects bloom-induced pH levels may impose on this cyanobacterium's competitors. Due to the pH-dependency of biosilicification processes, diatoms (which seasonally both precede and proceed Microcystis blooms in many fresh waters) may be unable to synthesize frustules at these pH levels. We assessed the effects of pH on the ecologically relevant diatom Fragilaria crotonensis in vitro, and on a Lake Erie diatom community in situ. In vitro assays revealed F. crotonensis monocultures exhibited lower growth rates and abundances when cultivated at a starting pH of 9.2 in comparison to pH 7.7. The suppressed growth trends in F. crotonensis were exacerbated when co-cultured with M. aeruginosa at pH conditions and cell densities that simulated a cyanobacteria bloom. Estimates demonstrated a significant decrease in silica (Si) deposition at alkaline pH in both in vitro F. crotonensis cultures and in situ Lake Erie diatom assemblages, after as little as 48 h of alkaline pH-exposure. These observations indicate elevated pH negatively affected growth rate and diatom silica deposition; in total providing a competitive disadvantage for diatoms. Our observations demonstrate pH likely plays a significant role in bloom succession, creating a potential to prolong summer Microcystis blooms and constrain diatom fall resurgence.

Keywords: CyanoHABs; Lake Erie; biogenic silica; diatoms; lake alkalinity; microcystis blooms.

FIGURE 1

Environmental data corresponding to a 2015 Lake Erie M. aeruginosa bloom. (A) Relative abundance (reported as percentage of total chlorophyll a) of diatoms (closed blue squares) and cyanobacteria (open blue circles) within the Lake Erie water column. (B) Average daily pH of the Lake Erie water column (closed blue triangles).

FIGURE 2

(A) In vitro F. crotonensis monoculture growth curves at pH 7.7 (black squares) and pH 9.2 (green squares). (B) F. crotonensis growth rate at pH 7.7 (black squares) and pH 9.2 (green squares). Statistically significant differences between pH treatments are denoted by p-values generated by Two-way ANOVAs. Standard error of the mean reported by error bars.

FIGURE 3

(A) In vitro F. crotonensis co-culture growth curves in a 10:1 ratio (F. crotonensis:M. aeruginosa) at pH 7.7 (black squares) and pH 9.2 (green squares). (B) F. crotonensis growth rate at 10:1 ratio (C) F. crotonensis growth curves in a 1:1 ratio (D) F. crotonensis growth rate in 1:1 ratio (E) F. crotonensis growth curves in a 1:10 ratio (F) F. crotonensis growth rate in a 1:10 ratio. Statistically significant differences between pH treatments are denoted by p-values generated by Two-way ANOVAs. Standard error of the mean reported by error bars.

FIGURE 4

Epifluorescent microscopy images (40x magnification) of F. crotonensis filaments after 48 h PDMPO incubations. Scale bar represents 25 μm. Chlorophyll a autofluorescence is depicted in red, and PDMPO fluorescence is in blue. (A,C,E) F. crotonensis cultures acclimated to pH 7.7. (B,D,F) F. crotonensis cultures acclimated to pH 9.2.

FIGURE 5

Si deposited per filament after 48 h PDMPO incubations in F. crotonensis cultures acclimated to pH 7.7 treatments (black squares) and pH 9.2 (green squares). Statistically significant differences are denoted by respective p-values generated by unpaired two-tailed t-tests. Standard error of the mean reported by error bars.

FIGURE 6

Si deposited per chl a concentration in pH 7.7 treatments (black squares), control pH 8.6 (gray squares), and pH 9.2 (green squares) after 48 h incubations. Statistically significant differences are denoted by respective p-values generated by One-way ANOVAs. Standard error of the mean reported by error bars.