Ecological mechanisms of sedimental microbial biodiversity shift and the role of antimicrobial resistance genes in modulating microbial turnover

Okugbe Ebiotubo Ohore; Yuwen Wang; Yunjie Wei; Edmond Sanganyado; Muhammad Shafiq; Xiaoyang Jiao; Amechi S Nwankwegu; Wenhua Liu; Zhen Wang

doi:10.1016/j.jenvman.2022.116547

Ecological mechanisms of sedimental microbial biodiversity shift and the role of antimicrobial resistance genes in modulating microbial turnover

J Environ Manage. 2023 Jan 1;325(Pt A):116547. doi: 10.1016/j.jenvman.2022.116547. Epub 2022 Oct 27.

Authors

Okugbe Ebiotubo Ohore¹, Yuwen Wang², Yunjie Wei², Edmond Sanganyado², Muhammad Shafiq³, Xiaoyang Jiao³, Amechi S Nwankwegu⁴, Wenhua Liu⁵, Zhen Wang⁶

Affiliations

¹ Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Protection, Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou, 515063, China. Electronic address: ohore@stu.edu.cn.
² Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Protection, Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou, 515063, China.
³ Department of Cell Biology and Genetics, Shantou University Medical College, Shantou, 515041, China.
⁴ College of Resources and Environment, Southwest University, Chongqing, 400716, China.
⁵ Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Protection, Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou, 515063, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, China.
⁶ Guangdong Provincial Key Laboratory of Marine Disaster Prediction and Protection, Guangdong Provincial Key Laboratory of Marine Biotechnology, Shantou University, Shantou, 515063, China. Electronic address: zhenwang@stu.edu.cn.

PMID: 36419283
DOI: 10.1016/j.jenvman.2022.116547

Abstract

The mechanisms of phylogenetic turnover of microbial communities to environmental perturbations in sediments remain unclear. In this study, the molecular mechanisms of phylogenetic turnover, and impact of antibiotics and antibiotic resistance genes (ARGs) on the modification of microbial assemblages were unravelled. We investigated 306 ARGs, 8 transposases, and 4 integron integrases, bacteria, and eukaryotic diversity through high-throughput quantitative PCR and illumina sequencing, 21 antibiotics and 3 tetracycline byproducts. The freshwater and estuary ecosystems were mainly dominated by genus Sulfurovum and colonised by closely related species compared with the estuary (closeness centrality = 0.42 vs. 0.46), which was dominated by genus Mycobacterium. Eighty-six percent of the ecological process in the bacterial community was driven by stochastic processes, while the rest was driven by deterministic processes. Environmental-related concentrations of antibiotics (0.15-32.53 ng/g) stimulated the proliferation of ARGs which potentially modulated the microbial community assembly. ARG acquisition significantly (P < 0.001) increased eukaryotic diversity through protection mechanisms. ARGs showed complex interrelationships with the microbial communities, and phylum arthropods and Nematea demonstrated the strongest ARG acquisition potential. This study provides key insights for environmental policymakers into understanding the ecological impact of antibiotics and the role of ARGs in modulating the phylogenetic turnover of microbial communities and trophic transfer mechanisms.

Keywords: Antibiotic byproducts; Antibiotic resistance genes; Arthropods; Microbial diversity; Phylogenetic turnover; Trophic transfer.

MeSH terms

Anti-Bacterial Agents* / analysis
Anti-Bacterial Agents* / pharmacology
Bacteria / genetics
Biodiversity
Drug Resistance, Bacterial
Genes, Bacterial
Microbiota*
Phylogeny
RNA, Ribosomal, 16S / genetics

Substances

Anti-Bacterial Agents
RNA, Ribosomal, 16S