Metagenomic insights into microalgae-bacterium-virus interactions and viral functions in phycosphere facing environmental fluctuations

Huiyuan Qi; Jiahui Lv; Jingqiu Liao; Junhao Jin; Yong Ren; Yi Tao; Dongsheng Wang; Pedro J J Alvarez; Pingfeng Yu

doi:10.1016/j.watres.2024.122676

Metagenomic insights into microalgae-bacterium-virus interactions and viral functions in phycosphere facing environmental fluctuations

Water Res. 2024 Oct 22;268(Pt A):122676. doi: 10.1016/j.watres.2024.122676. Online ahead of print.

Authors

Huiyuan Qi¹, Jiahui Lv², Jingqiu Liao³, Junhao Jin¹, Yong Ren⁴, Yi Tao⁵, Dongsheng Wang¹, Pedro J J Alvarez⁶, Pingfeng Yu⁷

Affiliations

¹ College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China.
² Shenzhen Key Laboratory of Ecological Remediation and Carbon Sequestration, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong, 518055, China; Guangdong Provincial Engineering Research Center for Urban Water Recycling and Environmental Safety, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong 518055, China; Guangdong Provincial Key Laboratory of Advanced Biomaterials, Department of Biomedical Engineering, Southern University of Science and Technology, Shenzhen, 518055, China.
³ Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA 24060, USA.
⁴ Shenzhen Key Laboratory of Ecological Remediation and Carbon Sequestration, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong, 518055, China; Guangdong Provincial Engineering Research Center for Urban Water Recycling and Environmental Safety, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong 518055, China.
⁵ Shenzhen Key Laboratory of Ecological Remediation and Carbon Sequestration, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong, 518055, China; Guangdong Provincial Engineering Research Center for Urban Water Recycling and Environmental Safety, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, Guangdong 518055, China. Electronic address: tao.yi@sz.tsinghua.edu.cn.
⁶ Department of Civil and Environmental Engineering and Rice WaTER Institute, Rice University, Houston, TX, 77005, USA.
⁷ College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China; Innovation Center of Yangtze River Delta, Zhejiang University, Jiashan 314100, China. Electronic address: yupf@zju.edu.cn.

PMID: 39471530
DOI: 10.1016/j.watres.2024.122676

Abstract

Despite the ecological and biotechnological significance of microalgae-bacterium symbionts, the response of host-virus interactions to external environmental fluctuations and the role of viruses in phycosphere remain largely unexplored. Herein, we employed algal-bacterial granular sludge (ABGS) with varying light intensity and organic carbon loading to investigate the mechanisms of microalgae-bacterium-virus symbionts in response to environmental fluctuations. Metagenomics revealed that enhanced light intensity decreased the diversity of microalgae, so did the diversity of symbiotic bacteria and viruses. As carbon sources decreased, bacteria prompted horizontal gene transfer in phycosphere by 12.76 %-157.40 %, increased the proportion of oligotrophs as keystone species (0.00 % vs 14.29 %) as well as viruses using oligotrophs as hosts (18.52 % vs 25.00 %). Furthermore, virus-carried auxiliary metabolic genes (AMGs) and biosynthetic gene clusters (BGCs) encoding vitamin B₁₂ synthesis (e.g., cobS), antioxidation (e.g., queC), and microbial aggregation (e.g., cysE). Additionally, phylogenetic and similarity analysis further revealed the evolutionary origin and potential horizontal transfer of the AMGs and BGCs, which could potentially enhance the adaptability of bacteria and eukaryotic microalgae. Overall, our research demonstrates that environmental fluctuations have cascading effects on the microalgae-bacteria-virus interactions, and emphasizes the important role of viruses in maintaining the stability of the phycosphere symbiotic community.

Keywords: Algal-bacterial symbionts; Auxiliary metabolic genes; Biosynthetic gene clusters; Horizontal gene transfer; Phycosphere; Viruses.