Climate warming promotes collateral antibiotic resistance development in cyanobacteria

Zhiyuan Wang; Qiuwen Chen; Jianyun Zhang; Huacheng Xu; Lingzhan Miao; Tao Zhang; Dongsheng Liu; Qiuheng Zhu; Hanlu Yan; Dandan Yan

doi:10.1016/j.watres.2024.121642

Climate warming promotes collateral antibiotic resistance development in cyanobacteria

Water Res. 2024 Apr 18:256:121642. doi: 10.1016/j.watres.2024.121642. Online ahead of print.

Authors

Zhiyuan Wang¹, Qiuwen Chen², Jianyun Zhang³, Huacheng Xu⁴, Lingzhan Miao⁵, Tao Zhang⁶, Dongsheng Liu⁶, Qiuheng Zhu⁶, Hanlu Yan⁷, Dandan Yan⁶

Affiliations

¹ National Key Laboratory of Water Disaster Prevention, Nanjing Hydraulic Research Institute, Nanjing 210098, China; Center for Eco-Environment Research, Nanjing Hydraulic Research Institute, Nanjing 210098, China; Yangtze Institute for Conservation and Development, Hohai University, Nanjing 210098, China.
² National Key Laboratory of Water Disaster Prevention, Nanjing Hydraulic Research Institute, Nanjing 210098, China; Center for Eco-Environment Research, Nanjing Hydraulic Research Institute, Nanjing 210098, China; Yangtze Institute for Conservation and Development, Hohai University, Nanjing 210098, China. Electronic address: qwchen@nhri.cn.
³ National Key Laboratory of Water Disaster Prevention, Nanjing Hydraulic Research Institute, Nanjing 210098, China; Yangtze Institute for Conservation and Development, Hohai University, Nanjing 210098, China. Electronic address: jyzhang@nhri.cn.
⁴ Nanjing Institute of Geography & Limnology, Chinese Academy of Sciences, Nanjing 210008, China.
⁵ College of Environment, Hohai University, Nanjing 210098, China.
⁶ Center for Eco-Environment Research, Nanjing Hydraulic Research Institute, Nanjing 210098, China.
⁷ National Key Laboratory of Water Disaster Prevention, Nanjing Hydraulic Research Institute, Nanjing 210098, China; Center for Eco-Environment Research, Nanjing Hydraulic Research Institute, Nanjing 210098, China.

PMID: 38657307
DOI: 10.1016/j.watres.2024.121642

Abstract

Both cyanobacterial blooms and antibiotic resistance have aggravated worldwide and posed a great threat to public health in recent years. As a significant source and reservoir of water environmental resistome, cyanobacteria exhibit confusing discrepancy between their reduced susceptibility and their chronic exposure to antibiotic mixtures at sub-inhibitory concentrations. How the increasing temperature affects the adaptive evolution of cyanobacteria-associated antibiotic resistance in response to low-level antibiotic combinations under climate change remains unclear. Here we profiled the antibiotic interaction and collateral susceptibility networks among 33 commonly detected antibiotics in 600 cyanobacterial strains isolated from 50 sites across four eutrophicated lakes in China. Cyanobacteria-associated antibiotic resistance level was found positively correlated to antibiotic heterogeneity across all sites. Among 528 antibiotic combinations, antagonism was observed for 62 % interactions and highly conserved within cyanobacterial species. Collateral resistance was detected in 78.5 % of pairwise antibiotic interaction, leading to a widened or shifted upwards mutant selection window for increased opportunity of acquiring second-step mutations. We quantified the interactive promoting effect of collateral resistance and increasing temperature on the evolution of both phenotypic and genotypic cyanobacteria-associated resistance under chronic exposure to environmental level of antibiotic combinations. With temperature increasing from 16 °C to 36 °C, the evolvability index and genotypic resistance level increased by 1.25 - 2.5 folds and 3 - 295 folds in the collateral-resistance-informed lineages, respectively. Emergence of resistance mutation pioneered by tolerance, which was jointly driven by mutation rate and persister fraction, was found to be accelerated by increased temperature and antibiotic switching rate. Our findings provided mechanic insights into the boosting effect of climate warming on the emergence and development of cyanobacteria-associated resistance against collateral antibiotic phenotypes.

Keywords: Antibiotic interaction; Collateral resistance; Cyanobacteria-associated antibiotic resistance; Resistance development; Temperature.