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Co-occurring microorganisms regulate the succession of cyanobacterial harmful algal blooms.
Environ Pollut. 2021 Nov 01; 288:117682.EP

Abstract

Cyanobacterial harmful algal blooms (CyanoHABs) have been found to transmit from N2 fixer-dominated to non-N2 fixer-dominated in many freshwater environments when the supply of N decreases. To elucidate the mechanisms underlying such "counter-intuitive" CyanoHAB species succession, metatranscriptomes (biotic data) and water quality-related variables (abiotic data) were analyzed weekly during a bloom season in Harsha Lake, a multipurpose lake that serves as a drinking water source and recreational ground. Our results showed that CyanoHABs in Harsha Lake started with N2-fixing Anabaena in June (ANA stage) when N was high, and transitioned to non-N2-fixing Microcystis- and Planktothrix-dominated in July (MIC-PLA stage) when N became limited (low TN/TP). Meanwhile, the concentrations of cyanotoxins, i.e., microcystins were significantly higher in the MIC-PLA stage. Water quality results revealed that N species (i.e., TN, TN/TP) and water temperature were significantly correlated with cyanobacterial biomass. Expression levels of several C- and N-processing-related cyanobacterial genes were highly predictive of the biomass of their species. More importantly, the biomasses of Microcystis and Planktothrix were also significantly associated with expressions of microbial genes (mostly from heterotrophic bacteria) related to processing organic substrates (alkaline phosphatase, peptidase, carbohydrate-active enzymes) and cyanophage genes. Collectively, our results suggest that besides environmental conditions and inherent traits of specific cyanobacterial species, the development and succession of CyanoHABs are regulated by co-occurring microorganisms. Specifically, the co-occurring microorganisms can alleviate the nutrient limitation of cyanobacteria by remineralizing organic compounds.

Authors+Show Affiliations

Department of Biological Sciences, Kent State University, Kent, OH, United States.Department of Biological Sciences, Kent State University, Kent, OH, United States.Division of Natural and Applied Sciences, Duke Kunshan University, Kunshan, China.U.S. Environmental Protection Agency, Office of Research and Development, Cincinnati, OH, United States.U.S. Environmental Protection Agency, Office of Research and Development, Cincinnati, OH, United States.U.S. Environmental Protection Agency, Office of Research and Development, Cincinnati, OH, United States. Electronic address: Lu.Jingrang@epa.gov.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

34271516

Citation

Wang, Kai, et al. "Co-occurring Microorganisms Regulate the Succession of Cyanobacterial Harmful Algal Blooms." Environmental Pollution (Barking, Essex : 1987), vol. 288, 2021, p. 117682.
Wang K, Mou X, Cao H, et al. Co-occurring microorganisms regulate the succession of cyanobacterial harmful algal blooms. Environ Pollut. 2021;288:117682.
Wang, K., Mou, X., Cao, H., Struewing, I., Allen, J., & Lu, J. (2021). Co-occurring microorganisms regulate the succession of cyanobacterial harmful algal blooms. Environmental Pollution (Barking, Essex : 1987), 288, 117682. https://doi.org/10.1016/j.envpol.2021.117682
Wang K, et al. Co-occurring Microorganisms Regulate the Succession of Cyanobacterial Harmful Algal Blooms. Environ Pollut. 2021 Nov 1;288:117682. PubMed PMID: 34271516.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Co-occurring microorganisms regulate the succession of cyanobacterial harmful algal blooms. AU - Wang,Kai, AU - Mou,Xiaozhen, AU - Cao,Huansheng, AU - Struewing,Ian, AU - Allen,Joel, AU - Lu,Jingrang, Y1 - 2021/07/08/ PY - 2021/01/14/received PY - 2021/06/10/revised PY - 2021/06/28/accepted PY - 2022/11/01/pmc-release PY - 2021/7/17/pubmed PY - 2021/9/30/medline PY - 2021/7/16/entrez KW - Bloom succession KW - CyanoHABs KW - Metatranscriptomics KW - Microbiome KW - Nitrogen limitation SP - 117682 EP - 117682 JF - Environmental pollution (Barking, Essex : 1987) JO - Environ Pollut VL - 288 N2 - Cyanobacterial harmful algal blooms (CyanoHABs) have been found to transmit from N2 fixer-dominated to non-N2 fixer-dominated in many freshwater environments when the supply of N decreases. To elucidate the mechanisms underlying such "counter-intuitive" CyanoHAB species succession, metatranscriptomes (biotic data) and water quality-related variables (abiotic data) were analyzed weekly during a bloom season in Harsha Lake, a multipurpose lake that serves as a drinking water source and recreational ground. Our results showed that CyanoHABs in Harsha Lake started with N2-fixing Anabaena in June (ANA stage) when N was high, and transitioned to non-N2-fixing Microcystis- and Planktothrix-dominated in July (MIC-PLA stage) when N became limited (low TN/TP). Meanwhile, the concentrations of cyanotoxins, i.e., microcystins were significantly higher in the MIC-PLA stage. Water quality results revealed that N species (i.e., TN, TN/TP) and water temperature were significantly correlated with cyanobacterial biomass. Expression levels of several C- and N-processing-related cyanobacterial genes were highly predictive of the biomass of their species. More importantly, the biomasses of Microcystis and Planktothrix were also significantly associated with expressions of microbial genes (mostly from heterotrophic bacteria) related to processing organic substrates (alkaline phosphatase, peptidase, carbohydrate-active enzymes) and cyanophage genes. Collectively, our results suggest that besides environmental conditions and inherent traits of specific cyanobacterial species, the development and succession of CyanoHABs are regulated by co-occurring microorganisms. Specifically, the co-occurring microorganisms can alleviate the nutrient limitation of cyanobacteria by remineralizing organic compounds. SN - 1873-6424 UR - https://www.unboundmedicine.com/medline/citation/34271516/Co_occurring_microorganisms_regulate_the_succession_of_cyanobacterial_harmful_algal_blooms_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0269-7491(21)01264-1 DB - PRIME DP - Unbound Medicine ER -