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Title: Quantification of microcystin production and biodegradation rates in the western basin of Lake Erie

Abstract

Abstract Cyanobacterial biomass forecasts currently cannot predict the concentrations of microcystin, one of the most ubiquitous cyanotoxins that threaten human and wildlife health globally. Mechanistic insights into how microcystin production and biodegradation by heterotrophic bacteria change spatially and throughout the bloom season can aid in toxin concentration forecasts. We quantified microcystin production and biodegradation during two growth seasons in two western Lake Erie sites with different physicochemical properties commonly plagued by summer Microcystis blooms. Microcystin production rates were greater with elevated nutrients than under ambient conditions and were highest nearshore during the initial phases of the bloom, and production rates were lower in later bloom phases. We examined biodegradation rates of the most common and toxic microcystin by adding extracellular stable isotope‐labeled microcystin‐LR (1  μ g L −1 ), which remained stable in the abiotic treatment (without bacteria) with minimal adsorption onto sediment, but strongly decreased in all unaltered biotic treatments, suggesting biodegradation. Greatest biodegradation rates (highest of −8.76 d −1 , equivalent to the removal of 99.98% in 18 h) were observed during peak bloom conditions, while lower rates were observed with lower cyanobacteria biomass. Cell‐specific nitrogen incorporation from microcystin‐LR by nanoscale imaging mass spectrometry showed that a small percentage of themore » heterotrophic bacterial community actively degraded microcystin‐LR. Microcystin production and biodegradation rates, combined with the microcystin incorporation by single cells, suggest that microcystin predictive models could be improved by incorporating toxin production and biodegradation rates, which are influenced by cyanobacterial bloom stage (early vs. late bloom), nutrient availability, and bacterial community composition.« less

Authors:
ORCiD logo [1];  [2];  [3];  [2];  [3];  [1];  [4];  [4];  [5];  [3];  [4]
  1. F.T. Stone Laboratory and Ohio Sea Grant The Ohio State University Put‐In‐Bay Ohio USA
  2. Lumigen Instrument Center Wayne State University Detroit Michigan USA
  3. Department of Biological Sciences Bowling Green State University Bowling Green Ohio USA
  4. Physical and Life Sciences Directorate Lawrence Livermore National Laboratory Livermore California USA
  5. Lake Erie Center University of Toledo Oregon Ohio USA
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1866304
Alternate Identifier(s):
OSTI ID: 1874111; OSTI ID: 1875319
Report Number(s):
LLNL-JRNL-827378
Journal ID: ISSN 0024-3590
Grant/Contract Number:  
AC52-07NA27344
Resource Type:
Published Article
Journal Name:
Limnology and Oceanography
Additional Journal Information:
Journal Name: Limnology and Oceanography Journal Volume: 67 Journal Issue: 7; Journal ID: ISSN 0024-3590
Publisher:
Wiley Blackwell (John Wiley & Sons)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cyanobacteria; Eutrophication; Microcystis; Microcystin-LR; NanoSIMS

Citation Formats

Chaffin, Justin D., Westrick, Judy A., Furr, Elliot, Birbeck, Johnna A., Reitz, Laura A., Stanislawczyk, Keara, Li, Wei, Weber, Peter K., Bridgeman, Thomas B., Davis, Timothy W., and Mayali, Xavier. Quantification of microcystin production and biodegradation rates in the western basin of Lake Erie. United States: N. p., 2022. Web. doi:10.1002/lno.12096.
Chaffin, Justin D., Westrick, Judy A., Furr, Elliot, Birbeck, Johnna A., Reitz, Laura A., Stanislawczyk, Keara, Li, Wei, Weber, Peter K., Bridgeman, Thomas B., Davis, Timothy W., & Mayali, Xavier. Quantification of microcystin production and biodegradation rates in the western basin of Lake Erie. United States. https://doi.org/10.1002/lno.12096
Chaffin, Justin D., Westrick, Judy A., Furr, Elliot, Birbeck, Johnna A., Reitz, Laura A., Stanislawczyk, Keara, Li, Wei, Weber, Peter K., Bridgeman, Thomas B., Davis, Timothy W., and Mayali, Xavier. Wed . "Quantification of microcystin production and biodegradation rates in the western basin of Lake Erie". United States. https://doi.org/10.1002/lno.12096.
@article{osti_1866304,
title = {Quantification of microcystin production and biodegradation rates in the western basin of Lake Erie},
author = {Chaffin, Justin D. and Westrick, Judy A. and Furr, Elliot and Birbeck, Johnna A. and Reitz, Laura A. and Stanislawczyk, Keara and Li, Wei and Weber, Peter K. and Bridgeman, Thomas B. and Davis, Timothy W. and Mayali, Xavier},
abstractNote = {Abstract Cyanobacterial biomass forecasts currently cannot predict the concentrations of microcystin, one of the most ubiquitous cyanotoxins that threaten human and wildlife health globally. Mechanistic insights into how microcystin production and biodegradation by heterotrophic bacteria change spatially and throughout the bloom season can aid in toxin concentration forecasts. We quantified microcystin production and biodegradation during two growth seasons in two western Lake Erie sites with different physicochemical properties commonly plagued by summer Microcystis blooms. Microcystin production rates were greater with elevated nutrients than under ambient conditions and were highest nearshore during the initial phases of the bloom, and production rates were lower in later bloom phases. We examined biodegradation rates of the most common and toxic microcystin by adding extracellular stable isotope‐labeled microcystin‐LR (1  μ g L −1 ), which remained stable in the abiotic treatment (without bacteria) with minimal adsorption onto sediment, but strongly decreased in all unaltered biotic treatments, suggesting biodegradation. Greatest biodegradation rates (highest of −8.76 d −1 , equivalent to the removal of 99.98% in 18 h) were observed during peak bloom conditions, while lower rates were observed with lower cyanobacteria biomass. Cell‐specific nitrogen incorporation from microcystin‐LR by nanoscale imaging mass spectrometry showed that a small percentage of the heterotrophic bacterial community actively degraded microcystin‐LR. Microcystin production and biodegradation rates, combined with the microcystin incorporation by single cells, suggest that microcystin predictive models could be improved by incorporating toxin production and biodegradation rates, which are influenced by cyanobacterial bloom stage (early vs. late bloom), nutrient availability, and bacterial community composition.},
doi = {10.1002/lno.12096},
journal = {Limnology and Oceanography},
number = 7,
volume = 67,
place = {United States},
year = {Wed May 04 00:00:00 EDT 2022},
month = {Wed May 04 00:00:00 EDT 2022}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1002/lno.12096

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Works referenced in this record:

The adsorption of microcystin-LR by natural clay particles
journal, February 2000


The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change
journal, February 2012


Grazing on Microcystis aeruginosa and degradation of microcystins by the heterotrophic flagellate Diphylleia rotans
journal, October 2013


The role of nitrogen and phosphorus in regulating Phormidium sp. (cyanobacteria) growth and anatoxin production
journal, February 2016

  • Heath, Mark; Wood, Susie A.; Young, Roger G.
  • FEMS Microbiology Ecology, Vol. 92, Issue 3
  • DOI: 10.1093/femsec/fiw021

Whole-Genome Sequencing of Bacterial Isolates That Degrade the Cyanobacterial Toxin Microcystin-LR
journal, October 2020

  • McCartney, Alexander T.; Yeo, Ji-Youn; Blomquist, Thomas M.
  • Microbiology Resource Announcements, Vol. 9, Issue 40
  • DOI: 10.1128/MRA.00959-20

Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil
journal, July 1998


Competition for Light between Toxic and Nontoxic Strains of the Harmful Cyanobacterium Microcystis
journal, March 2007

  • Kardinaal, W. E. A.; Tonk, L.; Janse, I.
  • Applied and Environmental Microbiology, Vol. 73, Issue 9
  • DOI: 10.1128/AEM.02892-06

Vertical distribution of buoyant Microcystis blooms in a Lagrangian particle tracking model for short-term forecasts in Lake Erie
journal, July 2016

  • Rowe, M. D.; Anderson, E. J.; Wynne, T. T.
  • Journal of Geophysical Research: Oceans, Vol. 121, Issue 7
  • DOI: 10.1002/2016JC011720

Cyanobacteria secondary metabolites-the cyanotoxins
journal, June 1992


Nitrogen Constrains the Growth of Late Summer Cyanobacterial Blooms in Lake Erie
journal, January 2013

  • Chaffin, Justin D.; Bridgeman, Thomas B.; Bade, Darren L.
  • Advances in Microbiology, Vol. 03, Issue 06
  • DOI: 10.4236/aim.2013.36A003

Biodegradation of microcystin-LR by indigenous mixed bacterial populations
journal, February 1996


Dissolved Microcystin Release Coincident with Lysis of a Bloom Dominated by Microcystis spp. in Western Lake Erie Attributed to a Novel Cyanophage
journal, October 2020

  • McKindles, Katelyn M.; Manes, Makayla A.; DeMarco, Jonathan R.
  • Applied and Environmental Microbiology, Vol. 86, Issue 22
  • DOI: 10.1128/AEM.01397-20

Metagenomic Identification of Bacterioplankton Taxa and Pathways Involved in Microcystin Degradation in Lake Erie
journal, April 2013


From River to Lake: Phosphorus partitioning and algal community compositional changes in Western Lake Erie
journal, March 2012

  • Bridgeman, Thomas B.; Chaffin, Justin D.; Kane, Douglas D.
  • Journal of Great Lakes Research, Vol. 38, Issue 1
  • DOI: 10.1016/j.jglr.2011.09.010

The Dilemma of Plants: To Grow or Defend
journal, September 1992

  • Herms, Daniel A.; Mattson, William J.
  • The Quarterly Review of Biology, Vol. 67, Issue 3
  • DOI: 10.1086/417659

Characterisation of a gene cluster involved in bacterial degradation of the cyanobacterial toxin microcystin LR
journal, January 2001

  • Bourne, David G.; Riddles, Peter; Jones, Gary J.
  • Environmental Toxicology, Vol. 16, Issue 6
  • DOI: 10.1002/tox.10013

Chlorophyll a as an indicator of microcystin: Short-term forecasting and risk assessment in Lake Erie
journal, November 2021


Isolation and characterization of Lake Erie bacteria that degrade the cyanobacterial microcystin toxin MC-LR
journal, February 2019


A space-time geostatistical model for probabilistic estimation of harmful algal bloom biomass and areal extent
journal, December 2019


Deciphering the effects of nitrogen, phosphorus, and temperature on cyanobacterial bloom intensification, diversity, and toxicity in western Lake Erie
journal, November 2018

  • Jankowiak, Jennifer; Hattenrath‐Lehmann, Theresa; Kramer, Benjamin J.
  • Limnology and Oceanography, Vol. 64, Issue 3
  • DOI: 10.1002/lno.11120

A Drinking Water Crisis in Lake Taihu, China: Linkage to Climatic Variability and Lake Management
journal, November 2009


Degradation of Multiple Peptides by Microcystin-Degrader Paucibacter toxinivorans (2C20)
journal, April 2021

  • Santos, Allan A.; Soldatou, Sylvia; de Magalhães, Valeria Freitas
  • Toxins, Vol. 13, Issue 4
  • DOI: 10.3390/toxins13040265

CLIMATE: Blooms Like It Hot
journal, April 2008


Challenges for mapping cyanotoxin patterns from remote sensing of cyanobacteria
journal, April 2016


Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms
journal, October 2010

  • Davis, Tw; Harke, Mj; Marcoval, Ma
  • Aquatic Microbial Ecology, Vol. 61, Issue 2
  • DOI: 10.3354/ame01445

The re-eutrophication of Lake Erie: Harmful algal blooms and hypoxia
journal, June 2016


Ecophysiological Examination of the Lake Erie Microcystis Bloom in 2014: Linkages between Biology and the Water Supply Shutdown of Toledo, OH
journal, June 2017

  • Steffen, Morgan M.; Davis, Timothy W.; McKay, R. Michael L.
  • Environmental Science & Technology, Vol. 51, Issue 12
  • DOI: 10.1021/acs.est.7b00856

Interactions between nitrogen form, loading rate, and light intensity on Microcystis and Planktothrix growth and microcystin production
journal, March 2018


Attachment between heterotrophic bacteria and microalgae influences symbiotic microscale interactions
journal, October 2018

  • Samo, Ty J.; Kimbrel, Jeffrey A.; Nilson, Daniel J.
  • Environmental Microbiology, Vol. 20, Issue 12
  • DOI: 10.1111/1462-2920.14357

The biodegradation of microcystins in temperate freshwater bodies with previous cyanobacterial history
journal, November 2017


Microcystin-LR Biodegradation by Bacillus sp.: Reaction Rates and Possible Genes Involved in the Degradation
journal, November 2016

  • Kansole, Michelline; Lin, Tsair-Fuh
  • Water, Vol. 8, Issue 11
  • DOI: 10.3390/w8110508

Permanganate Oxidation of Microcystin-LA: Kinetics, Quantification, and Implications for Effective Drinking Water Treatment
journal, May 2019

  • Szlag, David C.; Spies, Brian; Szlag, Regina G.
  • Journal of Toxicology, Vol. 2019
  • DOI: 10.1155/2019/3231473

A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp.
journal, April 2016


Natural Photodegradation of the Cyanobacterial Toxins Microcystin and Cylindrospermopsin
journal, March 2010

  • Wörmer, Lars; Huerta-Fontela, María; Cirés, Samuel
  • Environmental Science & Technology, Vol. 44, Issue 8
  • DOI: 10.1021/es9036012

Probabilistic forecast of microcystin toxin using satellite remote sensing, in situ observations and numerical modeling
journal, June 2020


The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms
journal, April 2016


Comparative Analysis of Microcystin Prevalence in Michigan Lakes by Online Concentration LC/MS/MS and ELISA
journal, January 2019

  • Birbeck, Johnna A.; Westrick, Judy A.; O’Neill, Grace M.
  • Toxins, Vol. 11, Issue 1
  • DOI: 10.3390/toxins11010013

Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa
journal, June 2006


Comparing MODIS and MERIS spectral shapes for cyanobacterial bloom detection
journal, June 2013


Bacterial communities' response to microcystins exposure and nutrient availability: Linking degradation capacity to community structure
journal, October 2013

  • Giaramida, Luca; Manage, Pathmalal M.; Edwards, Christine
  • International Biodeterioration & Biodegradation, Vol. 84
  • DOI: 10.1016/j.ibiod.2012.05.036

Light and the Transcriptional Response of the Microcystin Biosynthesis Gene Cluster
journal, August 2000


Degradation of the cyanobacterial hepatotoxin microcystin by aquatic bacteria
journal, January 1994

  • Jones, Gary J.; Bourne, David G.; Blakeley, Robert L.
  • Natural Toxins, Vol. 2, Issue 4
  • DOI: 10.1002/nt.2620020412

Assessment of the influence of key abiotic factors on the alternative microcystin degradation pathway(s) (mlr−): A detailed comparison with the mlr route (mlr+)
journal, December 2017


NanoSIP: NanoSIMS Applications for Microbial Biology
book, October 2021