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Physical drivers facilitating a toxigenic cyanobacterial bloom in a major Great Lakes tributary.

ABSTRACT: The Maumee River is the primary source for nutrients fueling seasonal Microcystis-dominated blooms in western Lake Erie's open waters though such blooms in the river are infrequent. The river also serves as source water for multiple public water systems and a large food services facility in northwest Ohio, USA. On 20 September 2017, an unprecedented bloom was reported in the Maumee River estuary within the Toledo metropolitan area, which triggered a recreational water advisory. Here we (1) explore physical drivers likely contributing to the bloom's occurrence, and (2) describe the toxin concentration and bacterioplankton taxonomic composition. A historical analysis using ten-years of seasonal river discharge, water level, and local wind data identified two instances when high-retention conditions occurred over ≥10 days in the Maumee River estuary: in 2016 and during the 2017 bloom. Observation by remote sensing imagery supported the advection of cyanobacterial cells into the estuary from the lake during 2017 and the lack of an estuary bloom in 2016 due to a weak cyanobacterial bloom in the lake. A rapid-response survey during the 2017 bloom determined levels of the cyanotoxins, specifically microcystins, in excess of recreational contact limits at sites within the lower 20 km of the river while amplicon sequencing found these sites were dominated by Microcystis. These results highlight the need to broaden our understanding of physical drivers of cyanobacterial blooms within the interface between riverine and lacustrine systems, particularly as such blooms are expected to become more prominent in response to a changing climate.

SUBMITTER: Matson PG

PROVIDER: S-EPMC7942401 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundPhosphonates are the main components in the global phosphorus redox cycle. Little is known about phosphonate metabolism in freshwater ecosystems, although rapid consumption of phosphonates has been observed frequently. Cyanobacteria are often the dominant primary producers in freshwaters; yet, only a few strains of cyanobacteria encode phosphonate-degrading (C-P lyase) gene clusters. The phycosphere is defined as the microenvironment in which extensive phytoplankton and heterotrophic bacteria interactions occur. It has been demonstrated that phytoplankton may recruit phycospheric bacteria based on their own needs. Therefore, the establishment of a phycospheric community rich in phosphonate-degrading-bacteria likely facilitates cyanobacterial proliferation, especially in waters with scarce phosphorus. We characterized the distribution of heterotrophic phosphonate-degrading bacteria in field Microcystis bloom samples and in laboratory cyanobacteria "phycospheres" by qPCR and metagenomic analyses. The role of phosphonate-degrading phycospheric bacteria in cyanobacterial proliferation was determined through coculturing of heterotrophic bacteria with an axenic Microcystis aeruginosa strain and by metatranscriptomic analysis using field Microcystis aggregate samples.ResultsAbundant bacteria that carry C-P lyase clusters were identified in plankton samples from freshwater Lakes Dianchi and Taihu during Microcystis bloom periods. Metagenomic analysis of 162 non-axenic laboratory strains of cyanobacteria (consortia cultures containing heterotrophic bacteria) showed that 20% (128/647) of high-quality bins from eighty of these consortia encode intact C-P lyase clusters, with an abundance ranging up to nearly 13%. Phycospheric bacterial phosphonate catabolism genes were expressed continually across bloom seasons, as demonstrated through metatranscriptomic analysis using sixteen field Microcystis aggregate samples. Coculturing experiments revealed that although Microcystis cultures did not catabolize methylphosphonate when axenic, they demonstrated sustained growth when cocultured with phosphonate-utilizing phycospheric bacteria in medium containing methylphosphonate as the sole source of phosphorus.ConclusionsThe recruitment of heterotrophic phosphonate-degrading phycospheric bacteria by cyanobacteria is a hedge against phosphorus scarcity by facilitating phosphonate availability. Cyanobacterial consortia are likely primary contributors to aquatic phosphonate mineralization, thereby facilitating sustained cyanobacterial growth, and even bloom maintenance, in phosphate-deficient waters. Video Abstract.

Project description:Colored dissolved organic matter (CDOM), a major component of the dissolved organic carbon (DOC) pool in many lakes, is an important controlling factor in lake ecosystem functioning. Absorption coefficients at 440 nm (a440, m-1), a common measure of CDOM, exhibited strong associations with dissolved iron (Fediss) and DOC in 280 lakes of the Upper Great Lakes States (UGLS: Minnesota, Wisconsin, and Michigan), as has been found in Scandinavia and elsewhere. Linear regressions between the three variables on UGLS lake data typically yielded R2 values of 0.6-0.9, suggesting that some underlying common processes influence organic matter and Fediss. Statistical and experimental evidence, however, supports only a minor role for iron contributions to a440 in UGLS lakes. Although both DOC and Fediss were significant variables in linear and log-log regressions on a440, DOC was the stronger predictor; adding Fediss to the linear a440-DOC model improved the R2 only from 0.90 to 0.93. Furthermore, experimental additions of FeIII to colored lake waters had only small effects on a440 (average increase of 0.242 m-1 per 100 μg/L of added FeIII). For 136 visibly stained waters (with a440 > 3.0 m-1), where allochthonous DOM predominates, DOM accounted for 92.3 ± 5.0% of the measured a440 values, and Fediss accounted for the remainder. In 75% of the lakes, Fediss accounted for < 10% of a440, but contributions of 15-30% were observed for 7 river-influenced lakes. Contributions of Fediss in UGLS lakes to specific UV absorbance at 254 nm (SUVA254) generally were also low. Although Fediss accounted for 5-10% of measured SUVA254 in a few samples, on average, 98.1% of the SUVA254 signal was attributable to DOM and only 1.9% to Fediss. DOC predictions from measured a440 were nearly identical to those from a440 corrected to remove Fediss contributions. Overall, variations in Fediss in most UGLS lakes have very small effects on CDOM optical properties, such as a440 and SUVA254, and negligible effects on the accuracy of DOC estimated from a440, data for which can be obtained at broad regional scales by remote sensing methods.

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Physical drivers facilitating a toxigenic cyanobacterial bloom in a major Great Lakes tributary.

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