Comamonas-dominant microbial community in carbon poor aquitard sediments revealed by metagenomic-based growth rate investigation

Miao Zhang; Bixi Zhao; Yuxi Yan; Zhanwen Cheng; Zengyi Li; Long Han; Yuqin Sun; Yan Zheng; Yu Xia

doi:10.1016/j.scitotenv.2023.169203

Comamonas-dominant microbial community in carbon poor aquitard sediments revealed by metagenomic-based growth rate investigation

Sci Total Environ. 2024 Feb 20:912:169203. doi: 10.1016/j.scitotenv.2023.169203. Epub 2023 Dec 10.

Authors

Miao Zhang¹, Bixi Zhao², Yuxi Yan¹, Zhanwen Cheng², Zengyi Li², Long Han², Yuqin Sun², Yan Zheng³, Yu Xia⁴

Affiliations

¹ School of Environment, Harbin Institute of Technology, Harbin 150001, China; School of Environmental Science and Engineering, College of Engineering, Southern University of Science and Technology, Shenzhen 518055, China.
² School of Environmental Science and Engineering, College of Engineering, Southern University of Science and Technology, Shenzhen 518055, China.
³ School of Environmental Science and Engineering, College of Engineering, Southern University of Science and Technology, Shenzhen 518055, China; State Environmental Protection Key Laboratory of Integrated Surface Water-Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China; Guangdong Provincial Key Laboratory of Soil and Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen, 518055, China. Electronic address: yan.zheng@sustech.edu.cn.
⁴ School of Environmental Science and Engineering, College of Engineering, Southern University of Science and Technology, Shenzhen 518055, China; State Environmental Protection Key Laboratory of Integrated Surface Water-Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, China; Guangdong Provincial Key Laboratory of Soil and Groundwater Pollution Control, School of Environmental Science and Engineering, Southern University of Science and Technology, Shenzhen, 518055, China. Electronic address: xiay@sustech.edu.cn.

PMID: 38086476
DOI: 10.1016/j.scitotenv.2023.169203

Abstract

The microbiological ecology of a low-nutrient shallow aquifer with high arsenic content in the Yinchuan Plain was investigated in this study. Amplicon sequencing data from five samples (depths: 1.5 m, 3.5 m, 11.2 m, 19.3 m, and 25.5 m) revealed diverse and adaptable microbial community. Among the microbial community, Comamonas was the most prominent, accounting for 10.52 % of the total. This genus displayed high growth rates, with a maximum growth rate of 12.06 d^-1 and a corresponding doubling time of 1.38 days, as determined through an analysis of codon usage bias. Functional annotation of Metagenome-Assembled Genomes (MAGs) for samples at 1.5 m and 11.2 m depths revealed Comamonas' metabolic versatility, including various carbon pathways, assimilative sulfate reduction (ASR), and dissimilatory reduction to ammonium (DNRA). The TPM (Transcripts Per Kilobase of exon model per Million mapped reads) of MAGs at 11.2 m sample was 15.7 and 12.3. The presence of arsenic resistance genes in Comamonas aligns with sediment arsenic levels (65.8 mg/kg for 1.5 m depth, 32.8 mg/kg for 11.2 m depth). This study highlights the role of Comamonas as a 'generalist' bacteria in challenging oligotrophic sediments, emphasizing the significance of such organisms in community stability and ecological functions. ENVIRONMENTAL IMPLICATION: Low-biomass limits the microbial activity and biogeochemical study in oligotrophic environments, which is the typical condition for underground aquatic ecosystems. Facilitated by growth rate estimation, our research focuses on active functional microorganisms and their biogeochemical metabolic in oligotrophic aquifer sediments, revealing their impact on the environment and response to arsenic threats. Findings illuminate the metabolic advantage of a 'generalist life-style' in carbon-scarce environments and contribute to a broader understanding of bacterial ecosystems and environmental impacts in oligotrophic aquifer sediments worldwide.

Keywords: Aquitard sediments; Comamonas genus; Growth rate; Microbial ecology; Oligotrophic environments.

MeSH terms

Arsenic* / analysis
Bacteria / metabolism
Carbon / metabolism
Geologic Sediments / chemistry
Metagenome
Microbiota*

Substances

Arsenic
Carbon