Microbiome Controls on Harmful Algal Toxin Production in Lake Erie

Xavier Mayali | 20-ERD-061

Project Overview

Freshwater Harmful Algal Blooms (HABs) are an increasing global concern and are caused by cyanobacteria that produce cyanotoxins, including a class of compounds known as microcystins. While the biomass of HABs can be predicted by the total amount of nutrients that flow into a freshwater ecosystem, the toxicity of blooms is not well understood and currently cannot be predicted in advance. One area that requires increasing research to better understand and ultimately predict HAB dynamics is how biological interactions in the Lake ecosystems drive bloom formation and decline, and how these interactions change under different nutrient conditions. This project aimed to increase our fundamental understanding of the ecological interactions between toxic cyanobacteria and their microbiome. Specifically, we examined the role of the cyanobacterial microbiome in impacting growth and cyanotoxin production under low inorganic nutrients to understand how microbial cycling of organic nutrients impact HABs. In addition, we developed a new approach to trace the degradation of cyanotoxins in a microbial ecosystem and used it to confirm microbial degradation in Lake Erie water.

Our main finding is that the cyanobacterial microbiome is strongly influenced by the availability of external inorganic and organic nutrients and has a variable impact on cyanobacterial growth and toxin accumulation. First, using experimental incubations of Lake Erie water with isotope labeled microcystin, we confirmed that microcystin degradation is mediated by a small proportion of the microbial community uniquely adapted to degrade microcystins and these cells incorporate nitrogen from the degraded toxin for growth. Next, using laboratory cultures and microbiome transplants, we demonstrated that the cyanobacterial microbiome can have a dual role in organic nitrogen cycling under low inorganic nitrogen conditions, in some cases competing with the cyanobacteria for uptake but in other cases providing additional nitrogen to increase total cyanotoxin production. In further work with laboratory cultures, we also examined the ability of the cyanobacterial microbiome to remineralize organic phosphorus for cyanobacterial growth, finding that certain microbiomes can degrade phosphonate compounds and allow cyanobacteria to proliferate and produce toxins. Finally, we quantified the direct competition between the microbiome and cyanobacteria for inorganic and inorganic nitrogen in Lake Erie over the course of a bloom to understand how different community members compete for nitrogen compounds.

Mission Impact

This project supports Lawrence Livermore National Laboratory's core competency in Bioscience and Bioengineering, as well as the Laboratory's misson focus area in Climate Impacts and Resilience. The U.S. Government, including the DOE and the NNSA, has identified that global climate change impacts pose a national security challenge and we must develop science and technology to meet this ongoing issue. One of the consequences of climate change is increased nutrient loading leading to high incidences of harmful algal blooms (HABs) in coasts and freshwaters. This research directly aims to tackle this issue by examining the biological factors that lead to the accumulation of cyanotoxins in freshwater ecosystems, using Lake Erie as an example. Beyond understanding the ecological interactions occurring during freshwater HABs, the possibility exists that enemies of the United States could develop weapons of mass destruction derived from these naturally occurring biotoxins. This research established a faster approach to detect microbial cyanotoxin degradation that could help future efforts to identify biological mitigation mechanisms to potential biotoxin attacks.

Publications, Presentations, and Patents 

X. Mayali, W. Li, P.K. Weber, J.D. Chaffin, K. Stanislawczyka, J.A. Westrick, E. Furr, L.A. Reitz, T.W. David, "Degradation of extracellular microcystin-LR by native lake bacterial communities" (Presentation, ASLO Aquatic Sciences Meeting, virtual, June 2021).

W Li, D. Baliu-Rodriguez, S.R. Rivera, S.H. Premathilaka, J.J. Kahrbush, J.A. Kimbrel, T.J. Samo, S. Isalilovic, G.J. Dick, "A single-cell view of organic nitrogen cycling in the cyanobacterial phycosphere" (Presentation, ASLO Aquatic Sciences Meeting, virtual, June 2021).

Smith D J, Kharbush J J, Davis T W, Kersten R D, Dick G J (2022). "Uptake of Phytoplankton-Derived Carbon and Cobalamins by Novel Acidobacteria Genera in Microcystis Blooms Inferred from Metagenomic and Metatranscriptomic Evidence." Applied and Environmental Microbiology. https://doi.org/10.1128/aem.01803-21

Baliu-Rodriguez D, Peraino N J, Premathilaka S H, Birbeck J A, Baliu-Rodriguez T, Westrick J A, Isailovic D. (2022). Identification of Novel Microcystins Using High-Resolution MS and MSn with Python Code. Environmental Science and Technology. https://doi.org/10.1021/acs.est.1c04296

Chaffin J, Westrick J, Furr E, Birbeck J, Reitz L, Stanislawczyk K, Li W, Weber P, Bridgeman T, Davis T, Mayali X .(2022). "Quantification of microcystin production and biodegradation rates in the western basin of Lake Erie." Limnology and Oceanography. https://doiorg/101002/lno12096

W. Li, S. Rivera, D. Baliu-Rodriguez, S. Premathilaka, S.Thenuwara, J. Kimbrel, J. Kharbush, T. Samo, D. Isailovic, G. Dick, X. Mayali, "New insights on organic nitrogen assimilation in Microcystis phycosphere and impacts on microcystin production" (Presentation, International Conference on Toxic Cyanobacteria, Toledo OH, 2022). 

X. Mayali, J.A. Kimbrel, W. Li, T.J. Samo, D. Isailovic, S. Premathilaka, J. Westrick, A.  Kung N. Peraino, P. Weber, "Do Microcystis laboratory cultures hold clues to bacterial microcystin degradation?" (Presentation, International Conference on Toxic Cyanobacteria, Toledo OH, 2022).