Abstract
Nitrite-dependent anaerobic methane oxidation (n-damo) acts as a crucial link between biogeochemical carbon and nitrogen cycles. Nevertheless, very few studies have characterized n-damo microorganisms in high-latitude permafrost regions. Therefore, this study investigated the vertical distribution and diversity of n-damo bacterial communities in soil from three forest types in the permafrost regions of the Daxing'an Mountains. A total of 11 and 8 operational taxonomic units (OTUs) of n-damo 16S rRNA and pmoA genes were observed, respectively. Remarkable spatial variations in n-damo bacteria community richness, diversity, and structure were observed at different soil depths. Moreover, the abundances of n-damo bacteria (16S rRNA and pmoA genes) varied between 1.55 × 104 to 1.47 × 105 and 1.31 × 103 to 3.11 × 104 copies g–1 dry soil (ds), as demonstrated by quantitative PCR analyses. 13CH4 stable isotope tracer assays indicated that the potential n-damo rates varied from 0 to 1.26 nmol g–1 day–1, with the middle layers (20–40 cm and 40–60 cm) exhibiting significantly higher values than the upper (0–20 cm) and deeper layers (80–100 cm) in all three forest types. Redundancy analyses (RDA) indicated that total organic carbon (TOC), nitrate (NO3––N), and nitrite (NO2––N) were key modulators of the distribution of n-damo bacterial communities. This study thus demonstrated the widespread occurrence of n-damo bacteria in cold and high-latitude regions of forest ecosystems and provided important insights into the global distribution of these bacteria.
Key points
• This study detected n-damo bacteria in soil samples obtained from the permafrost region of three forest types in the Daxing'an Mountains.
• The community composition of n-damo bacteria was mainly affected by soil depth and not forest type.
• The abundances of n-damo bacteria first increased and then decreased at higher soil depths.
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References
Adiya S, Dalantai S, Wu TH, Wu XD, Yamkhin J, Bao YH, Sumiya E, Yadamsuren G, Avirmed D, Dorjgotov B (2021) Spatial and temporal change patterns of near-surface CO2 and CH4 concentrations in different permafrost regions on the Mongolian Plateau from 2010 to 2017. Sci Total Environ 800:149433
Chen J, Zhou ZC, Gu JD (2014) Occurrence and diversity of nitrite-dependent anaerobic methane oxidation bacteria in the sediments of the South China Sea revealed by amplification of both 16S rRNA and pmoA genes. Appl Microbiol Biotechnol 98(12):5685–5696
Chen J, Zhou Z, Gu JD (2015) Complex community of nitrite-dependent anaerobic methane oxidation bacteria in coastal sediments of the Mai Po wetland by PCR amplification of both 16S rRNA and pmoA genes. Appl Microbiol Biotechnol 99(3):1463–1473
Chen S, Chen J, Chang S, Yi H, Huang DW, Xie SG, Guo QW (2018) Aerobic and anaerobic methanotrophic communities in urban landscape wetland. Appl Microbiol Biotechnol 102(1):433–445
Deutzmann JS, Schink B (2011) Anaerobic oxidation of methane in sediments of Lake Constance, an oligotrophic freshwater lake. Appl Environ Microbiol 77(13):4429–4436
Ettwig KF, Butler MK, Le Paslier DL, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJCT, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJM, Janssen-Megens EM, Francoijs K, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464(7288):543–548
Han P, Gu JD (2013) A newly designed degenerate PCR primer based on pmoA gene for detection of nitrite-dependent anaerobic methane-oxidizing bacteria from different ecological niches. Appl Microbiol Biotechnol 97(23):10155–10162
He ZF, Wang JQ, Hu JJ, Zhang H, Cai CY, Shen JX, Xu XH, Zheng P, Hu BL (2016) Improved PCR primers to amplify 16S rRNA genes from NC10 bacteria. Appl Microbiol Biotechnol 100(11):5099–5108
Holmes ME, Chanton JP, Tfaily MM, Ogram A (2015) CO2 and CH4 isotope compositions and production pathways in a tropical peatland. Glob Biogeochem Cycles 29(1):1–18
Hu BL, Shen LD, Lian X, Zhu Q, Liu S, Huang Q, He ZF, Geng S, Cheng DQ, Lou LP, Xu XY, Zheng P, He YF (2014) Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proc Natl Acad Sci USA 111(12):4495–4500
Jin HJ, Yu QH, Lü LZ, Guo DX, He RX, Yu SP, Sun GY, Li YW (2007) Degradation of permafrost in the Xing’anling Mountains, northeastern China. Permafrost Periglac 18(3):245–258
Jin HJ, Jin XY, He RX, Luo DL, Chang XL, Wang SL, Marchenko SS, Yang SZ, Yi CL, Li SJ, Harris SA (2019) Evolution of permafrost in China during the last 20 ka. Sci China Earth Sci 62(8):1207–1223
Long Y, Jiang XJ, Guo QW, Li BX, Xie SG (2017) Sediment nitrite-dependent methane-oxidizing microorganisms temporally and spatially shift in the Dongjiang River. Appl Microbiol Biotechnol 101(1):401–410
Luesken FA, Zhu BL, van Alen TA, Butler MK, Diaz MR, Song B, Op den Camp HJM, Jetten MSM, Ettwig KF (2011) PmoA primers for detection of anaerobic methanotrophs. Appl Environ Microbiol 77(11):3877–3880
Liu Y, Wang XY, Chen YJ, Zhang LR, Xu KL, Du Y (2020) Anaerobic methane-oxidizing bacterial communities in sediments of a drinking reservoir, Beijing, China. Ann Microbiol 70(1):1325–1346
Meng H, Wang YF, Chan HW, Wu RN, Gu JD (2016) Co-occurrence of nitrite-dependent anaerobic ammonium and methane oxidation processes in subtropical acidic forest soils. Appl Microbiol Biotechnol 100(17):7727–7739
Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damsté JSS, Op den Camp HJM, Jetten MSM, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440(7086):918–921
Shen LD, Liu S, Zhu Q, Li XY, Cai C, Cheng DQ, Lou LP, Xu XY, Zheng P, Hu BL (2014a) Distribution and diversity of nitrite-dependent anaerobic methane-oxidising bacteria in the sediments of the Qiantang River. Microb Ecol 67(2):341–349
Shen LD, Liu S, Huang Q, Lian X, He ZF, Geng S, Jin RC, He YF, Lou LP, Xu XY, Zheng P, Hu BL (2014b) Evidence for the cooccurrence of nitrite-dependent anaerobic ammonium and methane oxidation processes in a flooded paddy field. Appl Environ Microbiol 80(24):7611–7619
Shen LD, Wu HS, Gao ZQ (2015a) Distribution and environmental significance of nitrite-dependent anaerobic methane-oxidising bacteria in natural ecosystems. Appl Microbiol Biotechnol 99(1):133–142
Shen LD, Liu S, He ZF, Lian X, Huang Q, He YF, Lou LP, Xu XY, Zheng P, Hu BL (2015b) Depth-specific distribution and importance of nitrite-dependent anaerobic ammonium and methane-oxidising bacteria in an urban wetland. Soil Biol Biochem 83:43–51
Shen LD, Wu HS, Gao ZQ, Li J, Liu X (2016) Presence of diverse Candidatus Methylomirabilis oxyfera-like bacteria of NC10 phylum in agricultural soils. J Appl Microbiol 120(6):1552–1560
Shen LD, Ouyang L, Zhu YZ, Trimmer M (2019) Spatial separation of anaerobic ammonium oxidation and nitrite-dependent anaerobic methane oxidation in permeable riverbeds. Environ Microbiol 21(4):1185–1195
Wang Y, Zhu GB, Harhangi HR, Zhu BL, Jetten MSM, Yin CQ, Op den Camp HJM (2012) Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing bacteria in a paddy soil. FEMS Microbiol Lett 336(2):79–88
Wang Y, Huang P, Ye F, Jiang Y, Song LY, Op den Camp HJM, Zhu GB, Wu SJ (2016a) Nitrite-dependent anaerobic methane oxidizing bacteria along the water level fluctuation zone of the Three Gorges Reservoir. Appl Microbiol Biotechnol 100(4):1977–1986
Wang RF, Han XK, Lu PL, Yang QX (2016b) Co-occurrence and diversity of nitrite-dependent anaerobic methane oxidizing and anaerobic ammonium oxidizing bacteria in the water-level fluctuation zone of the three gorges reservoir, China. Fresen Environ Bull 25(12):5456–5466
Wang JQ, Shen LD, He ZF, Hu JJ, Cai ZY, Zheng P, Hu BL (2017) Spatial and temporal distribution of nitrite-dependent anaerobic methane-oxidizing bacteria in an intertidal zone of the East China sea. Appl Microbiol Biotechnol 101(21):8007–8014
Wang JQ, Cai CY, Li YF, Hua ML, Wang JR, Yang HR, Zheng P, Hu BL (2019) Denitrifying anaerobic methane oxidation: a previously overlooked methane sink in intertidal zone. Environ Sci Technol 53(1):203–212
Wang QK, Zhao XC, Chen LC, Yang QP, Chen S, Zhang WD (2018) Global synthesis of temperature sensitivity of soil organic carbon decomposition: latitudinal patterns and mechanisms. Funct Ecol 33(3):514–523
Xu S, Lu WJ, Mustafa MF, Caicedo LM, Guo HW, Fu XD, Wang HT (2017) Co-existence of anaerobic ammonium oxidation bacteria and denitrifying anaerobic methane oxidation bacteria in sewage sludge: community diversity and seasonal dynamics. Microb Ecol 74(4):832–840
Yan PZ, Li MC, Wei GS, Li H, Gao Z (2015) Molecular fingerprint and dominant environmental factors of nitrite-dependent anaerobic methane-oxidizing bacteria in sediments from the yellow river estuary, China. Plos One 10(9):0137996
Yang MX, Guo QW, Tong TL, Li NN, Xie SG, Long Y (2017) Vegetation type and layer depth influence nitrite-dependent methane-oxidizing bacteria in constructed wetland. Arch Microbiol 199(3):505–511
Zhang XW, Liu K, Li P, Jiao JJJ, Dvornyk V, Gu JD (2019) Molecular existence and diversity of nitrite-dependent anaerobic methane oxidizing (n-damo) bacteria in the lakes of badain of the Gobi Desert. Geomicrobiol J 36(6):522–531
Zheng YL, Hou LJ, Chen FY, Zhou J, Liu M, Yin GY, Gao J, Han P (2020) Denitrifying anaerobic methane oxidation in intertidal marsh soils: occurrence and environmental significance. Geoderma 357:113943
Zhou LL, Wang Y, Long XE, Guo JH, Zhu GB (2015) High abundance and diversity of nitrite-dependent anaerobic methane-oxidizing bacteria in a paddy field profile. FEMS Microbiol Lett 360(1):33–41
Zhong QP, Xue D, Chen H, Liu LF, He YX, Zhu D, He ZL (2020) Structure and distribution of nitrite-dependent anaerobic methane oxidation bacteria vary with water tables in Zoige peatlands. FEMS Microbiol Ecol 96(5):fiaa039
Zhu BL, van Dijk G, Fritz C, Smolders AJP, Pol A, Jetten MSM, Ettwig KF (2012) Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-dependent methane-oxidizing bacteria. Appl Environ Microbiol 78(24):8657–8665
Zhu GB, Zhou LL, Wang Y, Wang SY, Guo JH, Long XE, Sun XB, Jiang B, Hou QY, Jetten MSM, Yin CQ (2015) Biogeographical distribution of denitrifying anaerobic methane oxidizing bacteria in Chinese wetland ecosystems. Environ Microbiol Rep 7(1):128–138
Zhu GB, Wang MZ, Li YX, Wang Y, Fei HX, Wang SY (2018) Denitrifying anaerobic methane oxidizing in global upland soil: sporadic and non-continuous distribution with low influence. Soil Biol Biochem 119(1):90–100
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This study was supported by the National Natural Science Foundation of China (42171127) and Harbin Normal University Graduate Innovative Research Project (HSDSSCX2021-20).
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All the authors contributed to the study conception and design. D. M. conceived and designed the study. L. R., X. W., and X. L. performed the research and analyzed the data. L. R., L. L., and D. S. wrote the manuscript and all the authors revised the manuscript.
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Ren, L., Wu, X., Ma, D. et al. Nitrite-dependent anaerobic methane oxidation bacteria and potential in permafrost region of Daxing’an Mountains. Appl Microbiol Biotechnol 106, 743–754 (2022). https://doi.org/10.1007/s00253-021-11739-4
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DOI: https://doi.org/10.1007/s00253-021-11739-4