CRISPR-Cas phage defense systems and prophages in Candidatus Accumulibacter

Xuhan Deng; Jing Yuan; Liping Chen; Hang Chen; Chaohai Wei; Per H Nielsen; Stefan Wuertz; Guanglei Qiu

doi:10.1016/j.watres.2023.119906

CRISPR-Cas phage defense systems and prophages in Candidatus Accumulibacter

Water Res. 2023 May 15:235:119906. doi: 10.1016/j.watres.2023.119906. Epub 2023 Mar 23.

Authors

Xuhan Deng¹, Jing Yuan¹, Liping Chen¹, Hang Chen¹, Chaohai Wei², Per H Nielsen³, Stefan Wuertz⁴, Guanglei Qiu⁵

Affiliations

¹ School of Environment and Energy, South China University of Technology, Guangzhou 510006, China.
² School of Environment and Energy, South China University of Technology, Guangzhou 510006, China; The Key Lab of Pollution Control and Ecosystem Restoration in Industry Clusters, Ministry of Education, Guangzhou 510006, China.
³ Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore 637551, Singapore; Centre for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, Aalborg DK-9220, Denmark.
⁴ Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore 637551, Singapore; School of Civil and Environmental Engineering, Nanyang Technological University, Singapore 639798, Singapore. Electronic address: swuertz@ntu.edu.sg.
⁵ School of Environment and Energy, South China University of Technology, Guangzhou 510006, China; Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore 637551, Singapore; Guangdong Provincial Key Laboratory of Solid Wastes Pollution Control and Recycling, Guangzhou 510006, China. Electronic address: qiugl@scut.edu.cn.

PMID: 37004306
DOI: 10.1016/j.watres.2023.119906

Abstract

Candidatus Accumulibacter plays a major role in enhanced biological phosphorus removal (EBPR) from wastewater. Although bacteriophages have been shown to represent fatal threats to Ca. Accumulibacter organisms and thus interfere with the stability of the EBPR process, little is known about the ability of different Ca. Accumulibacter strains to resist phage infections. We conducted a systematic analysis of the occurrence and characteristics of clustered regularly interspaced short palindromic repeats and associated proteins (CRISPR-Cas) systems and prophages in Ca. Accumulibacter lineage members (43 in total, including 10 newly recovered genomes). Results indicate that 28 Ca. Accumulibacter genomes encode CRISPR-Cas systems. They were likely acquired via horizontal gene transfer, conveying a distinct adaptivity to phage predation to different Ca. Accumulibacter members. Major differences in the number of spacers show the unique phage resistance of these members. A comparison of the spacers in closely related Ca. Accumulibacter members from distinct geographical locations indicates that habitat isolation may have resulted in the acquisition of resistance to different phages by different Ca. Accumulibacter. Long-term operation of three laboratory-scale EBPR bioreactors revealed high relative abundances of Ca. Accumulibacter with CRISPSR-Cas systems. Their specific resistance to phages in these reactors was indicated by spacer analysis. Metatranscriptomic analyses showed the activation of the CRISPR-Cas system under both anaerobic and aerobic conditions. Additionally, 133 prophage regions were identified in 43 Ca. Accumulibacter genomes. Twenty-seven of them (in 19 genomes) were potentially active. Major differences in the occurrence of CRISPR-Cas systems and prophages in Ca. Accumulibacter will lead to distinct responses to phage predation. This study represents the first systematic analysis of CRISPR-Cas systems and prophages in the Ca. Accumulibacter lineage, providing new perspectives on the potential impacts of phages on Ca. Accumulibacter and EBPR systems.

Keywords: CRISPR-Cas systems; Candidatus Accumulibacter; Caudovirales; Enhanced biological phosphorus removal (EBPR); Prophages.

MeSH terms

Bacteriophages* / genetics
Betaproteobacteria*
CRISPR-Cas Systems
Phylogeny
Prophages / genetics
Wastewater

Substances

Wastewater