Abstract
Microcystins are potent hepatotoxins that are frequently detected in fresh water lakes plagued by toxic cyanobacteria. Microbial biodegradation has been referred to as the most important avenue for removal of microcystin from aquatic environments. The biochemical pathway most commonly associated with the degradation of microcystin is encoded by the mlrABCD (mlr) cassette. The ecological significance of this pathway remains unclear as no studies have examined the expression of these genes in natural environments. Six metatranscriptomes were generated from microcystin-producing Microcystis blooms and analyzed to assess the activity of this pathway in environmental samples. Seventy-eight samples were collected from Lake Erie, United States/Canada and Lake Tai (Taihu), China, and screened for the presence of mlr gene transcripts. Read mapping to the mlr cassette indicated transcripts for these genes were absent, with only 77 of the collective 3.7 billion reads mapping to any part of the mlr cassette. Analysis of the assembled metatranscriptomes supported this, with only distantly related sequences identified as mlrABC-like. These observations were made despite the presence of microcystin and over 500,000 reads mapping to the mcy cassette for microcystin production. Glutathione S-transferases and alkaline proteases have been previously hypothesized to be alternative pathways for microcystin biodegradation, and expression of these genes was detected across space and time in both lakes. While the activity of these alternative pathways needs to be experimentally confirmed, they may be individually or collectively more important than mlr genes in the natural environment. Importantly, the lack of mlr expression could indicate microcystin biodegradation was not occurring in the analyzed samples. This study raises interesting questions about the ubiquity, specificity and locality of microcystin biodegradation, and highlights the need for the characterization of relevant mechanisms in natural communities to understand the fate of microcystin in the environment and risk to public health.
Highlights
Microcystins (MCs) are the one of the most frequently detected cyanotoxins within freshwater harmful cyanobacterial blooms
Measurements of dissolved MC, particulate MC and chl a from 2015–2017 in Lake Erie indicated the presence of particulate MC and chl a corresponded to the presence of dissolved MC throughout blooms events (Supplementary Figure S1)
The capacity for MC biodegradation has been demonstrated in microbial communities from a variety of environments all over the world suggesting biodegradation of MCs is ubiquitous
Summary
Microcystins (MCs) are the one of the most frequently detected cyanotoxins within freshwater harmful cyanobacterial blooms (cyanoHABs). With cyanoHABS on the rise around the world, understanding the fate of MCs in the environment has assumed greater importance as they pose both ecological and public health risks. Conventional municipal water treatments are effective at removing or inactivating cyanobacterial cells, but the methods risk the release of MCs from the cell. MCs are not removed by flocculation processes and require secondary treatments that include the use of activated carbon, which is effective but costly (He et al, 2016). Cases of mortality and morbidity due to cyanotoxins have been reported since the 1800s involving birds, livestock, dogs, fish, and even humans (Chorus and Bartram, 1999; Wood, 2016). The number of cases has risen gradually over time and it is predicted that the number of individuals affected is greatly underestimated (Wood, 2016)
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