Comammox biogeography subject to anthropogenic interferences along a high-altitude river

Shufeng Liu; Hetong Cai; Xiaohui Zhao; Zongzhi Wu; Qian Chen; Xuming Xu; Sining Zhong; Weiling Sun; Jinren Ni

doi:10.1016/j.watres.2022.119225

Comammox biogeography subject to anthropogenic interferences along a high-altitude river

Water Res. 2022 Nov 1:226:119225. doi: 10.1016/j.watres.2022.119225. Epub 2022 Oct 8.

Authors

Shufeng Liu¹, Hetong Cai², Xiaohui Zhao³, Zongzhi Wu², Qian Chen⁴, Xuming Xu², Sining Zhong⁵, Weiling Sun⁶, Jinren Ni⁶

Affiliations

¹ College of Environmental Sciences and Engineering, Peking University; Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing, China. Electronic address: liushufeng@pku.edu.cn.
² College of Environmental Sciences and Engineering, Peking University; Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing, China.
³ College of Environmental Sciences and Engineering, Peking University; Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing, China; College of Water Resources and Hydropower Engineering, Xi'an University of Technology, Xi'an, China.
⁴ College of Environmental Sciences and Engineering, Peking University; Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing, China; State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, China. Electronic address: qianchen@pku.edu.cn.
⁵ College of Environmental Sciences and Engineering, Peking University; Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing, China; Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China.
⁶ College of Environmental Sciences and Engineering, Peking University; Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing, China; State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Peking University, Beijing, China; State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, China.

PMID: 36272199
DOI: 10.1016/j.watres.2022.119225

Abstract

The recent discovery of comammox Nitrospira performing complete ammonia oxidation to nitrate has overturned the long-held dogma of two-step nitrification on Earth, yet little is known about the effect of urbanization interference on their distribution. Using gene-centric metagenomics, we provided the first blueprints about comammox community, biogeography, and environmental drivers along a high-elevation (> 2000 m) river flowing through the largest city on the vulnerable Qinghai-Tibetan Plateau. Our study confirmed a wide presence and diversity of yet-uncultured comammox clade B across wet and dry seasons, with average 3.0 and 2.0 times as abundant as clade-A amoA genes in water and sediments, respectively. Species identified from freshwater and drinking water treatment plants dominated the comammox guilds (58∼100%), suggesting this plateau river shared a similar comammox assemblage with the above habitat types. Compared with the urban area harboring more abundant canonical Nitrospira identified in wastewater (average 24%), the upstream suburban reach had a smaller human population but larger proportions of comammox in ammonia-oxidizing prokaryotes (24∼72% of abundances) and Nitrospira sublineages I/II. Higher contents of nitrate and nitrite in water, and antibiotics in water and sediments, may restrain comammox niches in nitrifiers over the urban area. Further random forest analysis revealed that lincosamides and quinolones were the most important antibiotic predictors for the niche differentiations between comammox and canonical nitrifiers in water, while macrolides for those in sediments. Finally, by incubation experiments, we demonstrated higher activity contributions of benthic comammox in the suburban area (36.2∼92.8% of potential ammonia-oxidation rates) than in the urban reach, and that the contribution variation had significant negative relations with macrolides and their major components. Overall, this study highlighted that anthropogenic activities hampered the advantage of riverine complete nitrifiers over the canonical two-step ones.

Keywords: Qinghai-Tibetan Plateau; antibiotics; biogeographic pattern; complete nitrifier (comammox); gene-centric metagenomics; urbanization.

MeSH terms

Altitude
Ammonia*
Archaea* / genetics
Bacteria / genetics
Humans
Macrolides
Nitrates
Nitrification
Oxidation-Reduction
Phylogeny
Rivers

Substances

Ammonia
Nitrates
Macrolides