Award Abstract # 1736629
The role of heterotrophic bacteria in protecting cyanobacteria from hydrogen peroxide in coastal systems.

NSF Org: OCE
Division Of Ocean Sciences
Recipient: REGENTS OF THE UNIVERSITY OF MICHIGAN
Initial Amendment Date: July 11, 2017
Latest Amendment Date: July 11, 2017
Award Number: 1736629
Award Instrument: Standard Grant
Program Manager: Cynthia Suchman
csuchman@nsf.gov
 (703)292-2092
OCE
 Division Of Ocean Sciences
GEO
 Directorate For Geosciences
Start Date: January 1, 2018
End Date: December 31, 2022 (Estimated)
Total Intended Award Amount: $874,085.00
Total Awarded Amount to Date: $874,085.00
Funds Obligated to Date: FY 2017 = $874,085.00
History of Investigator:
  • Gregory Dick (Principal Investigator)
    gdick@umich.edu
  • George Kling (Co-Principal Investigator)
  • Rose Cory (Co-Principal Investigator)
Recipient Sponsored Research Office: Regents of the University of Michigan - Ann Arbor
1109 GEDDES AVE, SUITE 3300
ANN ARBOR
MI  US  48109-1079
(734)763-6438
Sponsor Congressional District: 06
Primary Place of Performance: University of Michigan Ann Arbor
1100 N University Ave
Ann Arbor
MI  US  48109-1005
Primary Place of Performance
Congressional District:
06
Unique Entity Identifier (UEI): GNJ7BBP73WE9
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY,
Chemical Oceanography
Primary Program Source: 01001718DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1670, 4444, 8555, 8811, 9117
Program Element Code(s): 1650, 1670
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Toxic cyanobacterial harmful algal blooms (CHABs) are now a worldwide problem that poses dangers for humans and aquatic organisms including life-threatening sickness, beach closures, health alerts, and drinking water treatment plant closures. This project focuses on the basic science needed to understand interactions between the microorganisms present in CHABs and the chemistry of the lakes they inhabit. In particular, it will study the sources, fate, and effects of hydrogen peroxide, which is a potentially important control on the toxicity and species present within these blooms. This research will be conducted in Lake Erie, a source of drinking water for 11 million people that is threatened by CHABs annually. Results will be directly integrated into two water quality models that are widely used by water managers and other stakeholders. This project will support the training of two PhD students, including a first-generation college attendee, and undergraduate students from backgrounds that are underrepresented in the earth sciences. Research will also be integrated into outreach aimed at increasing diversity in the earth sciences by involving women and underrepresented minorities in K-12 as well as college and adult educational settings.

The overall goal of this project is to determine the influence of hydrogen peroxide (H2O2) on cyanobacterial community composition and function in nearshore ecosystems. Preliminary results from Lake Erie show that dominant primary producers rely on heterotrophic bacteria to draw down H2O2 from transiently high environmental levels that are likely inhibitory to members of the cyanobacterial community. This suggests that H2O2 plays important and still poorly understood roles in aquatic microbial ecology. A combination of field sampling, experiments, and state-of-the art "-omics" will be used to test the overall hypothesis that H2O2 decomposition by heterotrophic "helpers" is an important determinant of microbial interactions and community structure and function. Lake Erie will be studied because (i) it is a model system for shallow coastal areas receiving high terrestrial nutrient runoff, (ii) it offers strong inshore-offshore gradients of light and nutrients for comparative studies, and (iii) existing sampling infrastructure, archived samples, and preliminary data can be leveraged. Field and laboratory experiments and measurements will be integrated to answer the following questions: Q1: What drives the temporal dynamics of H2O2 concentrations? Q2: Which enzymes and organisms are responsible for protecting the community via biological H2O2 decay? Q3: How does protection from H2O2 by helpers influence the composition and function of the community? The study will perform controlled lab experiments on cultures and on natural waters during different points of the bloom. Measures of H2O2 concentrations and rates of production and decay, along with supporting chemical and biological measurements, will be used to assess the major sources and sinks of H2O2. Molecular tools will be used to determine the pathways underpinning H2O2 decay and the effect of H2O2 on cyanobacterial community composition function. In parallel, impacts of varying H2O2 concentrations on growth rates of major cyanobacteria will be assessed experimentally. These experimental results will be placed into context through comparisons with the structure and function of microbial communities from field samples across spatial, temporal, and chemical gradients in this coastal ecosystem. The approach of integrating studies of H2O2 with "-omics" in natural systems is novel, and will advance our fundamental knowledge and understanding of the relationship between microbial community composition and function.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Kharbush, J and Smith, DJ and Powers, M and Vanderploeg, HA and Fanslow, D and Robinson, RL and Dick, GJ and Pearson, A "Chlorophyll nitrogen isotope values track shifts between cyanobacteria and eukaryotic algae in a natural phytoplankton community in Lake Erie" Organic geochemistry , v.128 , 2019 doi.org/10.1016/j.orggeochem.2018.12.006 Citation Details
Yancey, Colleen E. and Kiledal, E. Anders and Chaganti, Subba Rao and Denef, Vincent J. and Errera, Reagan M. and Evans, Jacob T. and Hart, Lauren N. and Isailovic, Dragan and James, William S. and Kharbush, Jenan K. and Kimbrel, Jeffrey A. and Li, Wei an "The Western Lake Erie Culture Collection: A promising resource for evaluating the physiological and genetic diversity of Microcystis and its associated microbiome" Harmful Algae , 2023 https://doi.org/10.1016/j.hal.2023.102440 Citation Details
Pandey, Dhurba Raj and Polik, Catherine and Cory, Rose M. "Controls on the photochemical production of hydrogen peroxide in Lake Erie" Environmental Science: Processes & Impacts , v.24 , 2022 https://doi.org/10.1039/d2em00327a Citation Details
Smith, Derek J. and Berry, Michelle A. and Cory, Rose M. and Johengen, Thomas H. and Kling, George W. and Davis, Timothy W. and Dick, Gregory J. "Heterotrophic Bacteria Dominate Catalase Expression during Microcystis Blooms" Applied and Environmental Microbiology , v.88 , 2022 https://doi.org/10.1128/aem.02544-21 Citation Details
Smith, Derek J. and Kharbush, Jenan J. and Kersten, Roland D. and Dick, Gregory J. "Uptake of Phytoplankton-Derived Carbon and Cobalamins by Novel Acidobacteria Genera in Microcystis Blooms Inferred from Metagenomic and Metatranscriptomic Evidence" Applied and Environmental Microbiology , v.88 , 2022 https://doi.org/10.1128/aem.01803-21 Citation Details
Hellweger, Ferdi L. and Martin, Robbie M. and Eigemann, Falk and Smith, Derek J. and Dick, Gregory J. and Wilhelm, Steven W. "Models predict planned phosphorus load reduction will make Lake Erie more toxic" Science , v.376 , 2022 https://doi.org/10.1126/science.abm6791 Citation Details
Dick, Gregory J. and Duhaime, Melissa B. and Evans, Jacob T. and Errera, Reagan M. and Godwin, Casey M. and Kharbush, Jenan J. and Nitschky, Helena S. and Powers, McKenzie A. and Vanderploeg, Henry A. and Schmidt, Kathryn C. and Smith, Derek J. and Yancey "The genetic and ecophysiological diversity of Microcystis" Environmental Microbiology , v.23 , 2021 https://doi.org/10.1111/1462-2920.15615 Citation Details
Smith, Derek J. and Tan, James Y. and Powers, McKenzie A. and Lin, Xiaoxia N. and Davis, Timothy W. and Dick, Gregory J. "Individual Microcystis colonies harbour distinct bacterial communities that differ by Microcystis oligotype and with time" Environmental Microbiology , v.23 , 2021 https://doi.org/10.1111/1462-2920.15514 Citation Details
Schmidt, Kathryn C. and Jackrel, Sara L. and Smith, Derek J. and Dick, Gregory J. and Denef, Vincent J. "Genotype and host microbiome alter competitive interactions between Microcystis aeruginosa and Chlorella sorokiniana" Harmful Algae , v.99 , 2020 https://doi.org/10.1016/j.hal.2020.101939 Citation Details

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Toxic cyanobacterial harmful algal blooms (CHABs) threaten freshwater systems worldwide, posing dangers including disruption of ecosystems, human illness, beach closures, and unsafe drinking water. This project conducted research to understand interactions between the microorganisms present in CHABs and the chemistry of the lakes they inhabit. In particular, it focused on the sources, fate, and effects of hydrogen peroxide, which may control the toxicity and microbial species present within these blooms. The overall goal of this project was to determine the influence of hydrogen peroxide on cyanobacterial community composition and toxicity. The research was carried out in Lake Erie, a source of drinking water for 11 million people that is threatened by CHABs that are dominated by Microcystis, a globally distributed cyanobacterium that produces the toxin microcystin.

 

Field work was conducted on ~weekly research cruises from June to October in 2018-2022 in collaboration with the Cooperative Institute for Great Lakes Research and the NOAA Great Lakes Environmental Research Laboratory. This produced a valuable dataset on the seasonal and interannual variability of hydrogen peroxide concentrations and microbial community composition and also provided samples for laboratory experiments to quantify the sources, fate, and effects of hydrogen peroxide. Hydrogen peroxide concentrations frequently reached levels that are known to inhibit growth of cyanobacteria and other microorganisms, consistent with the idea that hydrogen peroxide has an important effect on microbial communities.

 

Results from experiments indicate that hydrogen peroxide was produced by both photochemistry (in which sunlight reacts with colored dissolved organic matter) and biological processes (photosynthesis and respiration). Rates of hydrogen peroxide production varied across space (including nearshore to offshore) and time (within and between years). Photochemical production of hydrogen peroxide depended on the composition of colored dissolved organic matter, which varied spatially and temporally. Biological production of hydrogen peroxide was largely dependent on light and small particles and was correlated with bacterial community composition, consistent with an important role of bacterial processing of organic carbon molecules generated during photosynthesis. Bacteria were also responsible for the degradation of hydrogen peroxide through peroxidase and catalase enzymes. Overall, these results show that bacteria exert strong control over hydrogen peroxide concentrations and influence the cyanobacterial community composition in Western Lake Erie.     

 

Genomic methods were used to investigate the interactions between Microcystis and bacteria. Microorganisms physically associated with Microcystis were distinct from surrounding bulk water and correlated with sampling time and Microcystis strain, suggesting that environmental conditions or symbiotic interactions strongly influence Microcystis-associated microbial communities. Results also indicated the exchange of metabolites between heterotrophic bacteria and Microcystis. Taken together with evidence that the heterotrophic bacteria degrade hydrogen peroxide, thus protecting Microcystis from oxidative stress, these results suggest a mutualistic symbiotic relationship between Microcystis and these “helper” bacteria.

 

Results were integrated into a model that was used to predict the outcome of current nutrient management practices for Western Lake Erie. The results of this modeling study suggest that the proposed reduction of phosphorus inputs into Western Lake Erie could result in an increase in the concentration of microcystin due to an increase in the availability of nitrogen and light, which produces hydrogen peroxide. Both high nitrogen availability and hydrogen peroxide are thought to stimulate toxin production by favoring toxin-producing strains of Microcystis. However, subsequent lab experiments and genome sequencing also showed that Microcystis strains are highly diverse and that hydrogen peroxide does not always favor toxin-producing strains of Microcystis; more research is needed to understand this complexity and update models accordingly.

 

Results of this project were described in 9 peer-reviewed scientific publications, with at least two more forthcoming, and in numerous oral presentations at scientific conferences and to various stakeholders. These results have improved our understanding of how environmental conditions shape production of toxins from harmful algal blooms that threaten drinking water supplies. Thus, there is a potential impact of this research on the important societal issues of water quality, drinking water security, and harmful algal blooms.

 

Overall, the project trained and provided professional development opportunities for 5 graduate students, 11 undergraduate students, 3 postdocs, and 3 technicians, including training in field and laboratory methods as well as bioinformatics and omics analysis. Research was integrated into undergraduate and graduate coursework at the University of Michigan as well as outreach to increase diversity in the earth sciences by involving women and underrepresented minorities in K-12 as well as college and adult educational settings.

 


Last Modified: 04/30/2023
Modified by: Gregory J Dick

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