Bacterial community shifts induced by high concentration hydrogen peroxide treatment of Microcystis bloom in a mesocosm study

Abstract

Hydrogen peroxide has gained popularity as an environmentally friendly treatment for cyanobacterial harmful algal blooms (cHABs) that takes advantage of oxidative stress sensitivity in cyanobacteria at controlled concentrations. Higher concentrations of hydrogen peroxide treatments may seem appealing for more severe cHABs but there is currently little understanding of the environmental impacts of this approach. Of specific concern is the associated microbial community, which may play key roles in the succession/recovery process post-treatment. To better understand impacts of a high concentration treatment on non-target microbial communities, we applied a hydrogen peroxide spray equating to a total volume concentration of 14 mM (473 mg/L, 0.04%) to 250 L mesocosms containing Microcystis bloom biomass, monitoring treatment and control mesocosms for 4 days. Cyanobacteria dominated control mesocosms throughout the experiment while treatment mesocosms experienced a 99% reduction, as determined by bacterial amplicon sequencing, and a 92% reduction in bacterial cell density within 1 day post-treatment. Only the bacterial community exhibited signs of regrowth, with a fold change of 9.2 bacterial cell density from day 1 to day 2. Recovery consisted of succession by Planctomycetota (47%) and Gammaproteobacteria (17%), which were likely resilient due to passive cell component compartmentalization and rapid upregulation of dnaK and groEL oxidative stress genes, respectively. The altered microbiome retained beneficial functionality of microcystin degradation through a currently recognized but unidentified pathway in Gammaproteobacteria, resulting in a 70% reduction coinciding with bacterial regrowth. There was also an 81% reduction of both total nitrogen and phosphorus, as compared to 91 and 93% in the control, respectively, due to high expressions of genes related to nitrogen (argH, carB, glts, glnA) and phosphorus (pntAB, phoB, pstSCB) cycling. Overall, we found a portion of the bacterial community was resilient to the high-concentration hydrogen peroxide treatment, resulting in Planctomycetota and Gammaproteobacteria dominance. This high-concentration treatment may be suitable to rapidly end cHABs which have already negatively impacted the aquatic environment rather than allow them to persist.

Keywords: Cyanobacteria; Metatranscriptomics; Microbiome; cHAB.