Vertical Distribution of Candidatus Methylomirabilis and Methanoperedens in Agricultural Soils

Overview

Journal Appl Microbiol Biotechnol

Specialties Biomedical Engineering
Biotechnology
Microbiology

Date 2024 Jan 4

PMID 38175239

Authors

Lidong Shen

Yefan He

Qinan Hu

Yuling Yang

Bingjie Ren

Wangting Yang

Caiyu Geng

Jinghao Jin

Yanan Bai

Affiliations

Soon will be listed here.

Abstract

Candidatus Methylomirabilis-related bacteria conduct anaerobic oxidation of methane (AOM) coupling with NO reduction, and Candidatus Methanoperedens-related archaea perform AOM coupling with reduction of diverse electron acceptors, including NO, Fe (III), Mn (IV) and SO. Application of nitrogen fertilization favors the growth of these methanotrophs in agricultural fields. Here, we explored the vertical variations in community structure and abundance of the two groups of methanotrophs in a nitrogen-rich vegetable field via using illumina MiSeq sequencing and quantitative PCR. The retrieved Methylomirabilis-related sequences had 91.12%-97.32% identity to the genomes of known Methylomirabilis species, and Methanoperedens-related sequences showed 85.49%-97.48% identity to the genomes of known Methanoperedens species which are capable of conducting AOM coupling with reduction of NO or Fe (III). The Methanoperedens-related archaeal diversity was significantly higher than Methylomirabilis-related bacteria, with totally 74 and 16 operational taxonomic units, respectively. In contrast, no significant difference in abundance between the bacteria (9.19 × 10-3.83 × 10 copies g dry soil) and the archaea (1.55 × 10-3.24 × 10 copies g dry soil) was observed. Furthermore, the abundance of both groups of methanotrophs exhibited a strong vertical variation, which peaked at 30-40 and 20-30 cm layers, respectively. Soil water content and pH were the key factors influencing Methylomirabilis-related bacterial diversity and abundance, respectively. For the Methanoperedens-related archaea, both soil pH and ammonium content contributed significantly to the changes of these archaeal diversity and abundance. Overall, we provide the first insights into the vertical distribution and regulation of Methylomirabilis-related bacteria and Methanoperedens-related archaea in vegetable soils. KEY POINTS: • The archaeal diversity was significantly higher than bacterial. • There was no significant difference in the abundance between bacteria and archaea. • The abundance of bacteria and archaea peaked at 30-40 and 20-30 cm, respectively.

References

Cai C, Leu A, Xie G, Guo J, Feng Y, Zhao J . A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction. ISME J. 2018; 12(8):1929-1939. PMC: 6052012. DOI: 10.1038/s41396-018-0109-x. View

Chen F, Zheng Y, Hou L, Niu Y, Gao D, An Z . Microbial abundance and activity of nitrite/nitrate-dependent anaerobic methane oxidizers in estuarine and intertidal wetlands: Heterogeneity and driving factors. Water Res. 2020; 190:116737. DOI: 10.1016/j.watres.2020.116737. View

Chen F, Zheng Y, Hou L, Zhou J, Yin G, Liu M . Denitrifying anaerobic methane oxidation in marsh sediments of Chongming eastern intertidal flat. Mar Pollut Bull. 2019; 150:110681. DOI: 10.1016/j.marpolbul.2019.110681. View

Chen L, Li L, Zhang S, Zhang W, Xue K, Wang Y . Anaerobic methane oxidation linked to Fe(III) reduction in a Candidatus Methanoperedens-enriched consortium from the cold Zoige wetland at Tibetan Plateau. Environ Microbiol. 2021; 24(2):614-625. DOI: 10.1111/1462-2920.15848. View

Ettwig K, Butler M, Le Paslier D, Pelletier E, Mangenot S, Kuypers M . Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature. 2010; 464(7288):543-8. DOI: 10.1038/nature08883. View

Ettwig K, van Alen T, van de Pas-Schoonen K, Jetten M, Strous M . Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol. 2009; 75(11):3656-62. PMC: 2687271. DOI: 10.1128/AEM.00067-09. View

Graf J, Mayr M, Marchant H, Tienken D, Hach P, Brand A . Bloom of a denitrifying methanotroph, 'Candidatus Methylomirabilis limnetica', in a deep stratified lake. Environ Microbiol. 2018; 20(7):2598-2614. DOI: 10.1111/1462-2920.14285. View

Haroon M, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P . Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature. 2013; 500(7464):567-70. DOI: 10.1038/nature12375. View

He F, Jiang R, Chen Q, Zhang F, Su F . Nitrous oxide emissions from an intensively managed greenhouse vegetable cropping system in Northern China. Environ Pollut. 2009; 157(5):1666-72. DOI: 10.1016/j.envpol.2008.12.017. View

10.

He Z, Cai C, Wang J, Xu X, Zheng P, Jetten M . A novel denitrifying methanotroph of the NC10 phylum and its microcolony. Sci Rep. 2016; 6:32241. PMC: 5007514. DOI: 10.1038/srep32241. View

11.

Huang T, Liu W, Zhang Y, Zhou Q, Wu Z, He F . A stable simultaneous anammox, denitrifying anaerobic methane oxidation and denitrification process in integrated vertical constructed wetlands for slightly polluted wastewater. Environ Pollut. 2020; 262:114363. DOI: 10.1016/j.envpol.2020.114363. View

12.

Leu A, Cai C, McIlroy S, Southam G, Orphan V, Yuan Z . Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae. ISME J. 2020; 14(4):1030-1041. PMC: 7082337. DOI: 10.1038/s41396-020-0590-x. View

13.

Long Y, Jiang X, Guo Q, Li B, Xie S . Sediment nitrite-dependent methane-oxidizing microorganisms temporally and spatially shift in the Dongjiang River. Appl Microbiol Biotechnol. 2016; 101(1):401-410. DOI: 10.1007/s00253-016-7888-7. View

14.

Luo D, Meng X, Zheng N, Li Y, Yao H, Chapman S . The anaerobic oxidation of methane in paddy soil by ferric iron and nitrate, and the microbial communities involved. Sci Total Environ. 2021; 788:147773. DOI: 10.1016/j.scitotenv.2021.147773. View

15.

Mayr M, Zimmermann M, Guggenheim C, Brand A, Burgmann H . Niche partitioning of methane-oxidizing bacteria along the oxygen-methane counter gradient of stratified lakes. ISME J. 2019; 14(1):274-287. PMC: 6908591. DOI: 10.1038/s41396-019-0515-8. View

16.

Nie W, Ding J, Xie G, Tan X, Lu Y, Peng L . Simultaneous nitrate and sulfate dependent anaerobic oxidation of methane linking carbon, nitrogen and sulfur cycles. Water Res. 2021; 194:116928. DOI: 10.1016/j.watres.2021.116928. View

17.

Niu Y, Zheng Y, Hou L, Gao D, Chen F, Pei C . Microbial dynamics and activity of denitrifying anaerobic methane oxidizers in China's estuarine and coastal wetlands. Sci Total Environ. 2021; 806(Pt 1):150425. DOI: 10.1016/j.scitotenv.2021.150425. View

18.

Shen L, Tian M, Cheng H, Liu X, Yang Y, Liu J . Different responses of nitrite- and nitrate-dependent anaerobic methanotrophs to increasing nitrogen loading in a freshwater reservoir. Environ Pollut. 2021; 263(Pt A):114623. DOI: 10.1016/j.envpol.2020.114623. View

19.

He D, Guo Z, Shen W, Ren L, Sun D, Yao Q . Fungal Communities Are More Sensitive to the Simulated Environmental Changes than Bacterial Communities in a Subtropical Forest: the Single and Interactive Effects of Nitrogen Addition and Precipitation Seasonality Change. Microb Ecol. 2022; 86(1):521-535. DOI: 10.1007/s00248-022-02092-8. View

20.

Shen L, Liu S, Huang Q, Lian X, He Z, Geng S . Evidence for the cooccurrence of nitrite-dependent anaerobic ammonium and methane oxidation processes in a flooded paddy field. Appl Environ Microbiol. 2014; 80(24):7611-9. PMC: 4249227. DOI: 10.1128/AEM.02379-14. View