The facilitating role of phycospheric heterotrophic bacteria in cyanobacterial phosphonate availability and Microcystis bloom maintenance

Microbiome

Research

Jin Lv¹  Bo-Ping Han²  Jerry J. Brand³  Xin-Yi Li⁴  Meng-Yun Chen⁴  Yong-Hui Gong⁴  Ying Zeng⁴  Wen-Sheng Shu⁵  Liang Zhao⁶  Ting Chen⁷  Wen-Kai Teng⁸  Nan-Qin Gan⁹  Li-Zhou Lin^1,10  Li-Rong Song^1,11  Ling-Ling Zheng^1,11 

[1] Analysis and Testing Center, South China Normal University, 510631, Guangzhou, People’s Republic of China;Department of Ecology and Institute of Hydrobiology, Jinan University, 510632, Guangzhou, People’s Republic of China;Department of Molecular Biosciences and the Culture Collection of Algae, University of Texas at Austin, 78712, Austin, TX, USA;Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, 510631, Guangzhou, People’s Republic of China;Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, 510631, Guangzhou, People’s Republic of China;Guangdong Magigene Biotechnology Co., Ltd., 518081, Shenzhen, People’s Republic of China;Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, 510631, Guangzhou, People’s Republic of China;State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, 430072, Wuhan, People’s Republic of China;Institute for Artificial Intelligence and Department of Computer Science and Technology, Tsinghua University, 100084, Beijing, People’s Republic of China;State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, 510275, Guangzhou, People’s Republic of China;State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, 430072, Wuhan, People’s Republic of China;State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, 430072, Wuhan, People’s Republic of China;Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, State Key Laboratory of Applied Microbiology Southern China, Institute of Microbiology, Guangdong Academy of Sciences, 510070, Guangzhou, People’s Republic of China;State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, 430072, Wuhan, People’s Republic of China;National Aquatic Biological Resource Center, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, People’s Republic of China;

关键词: Cyanobacteria;    Microcystis;    Phytoplankton-bacteria interaction;    Phosphonate degradation;   

DOI  :  10.1186/s40168-023-01582-2

 received in 2022-03-16, accepted in 2023-05-23,  发布年份 2023

来源: Springer

【 摘 要 】

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.CDjGUzfe77vQSL5wxbu5DEVideo Abstract

【 授权许可】

CC BY   
© The Author(s) 2023

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