Abstract
Water is essential for life on Earth, and an important medium for microbial energy and metabolism. Dormancy is a state of low metabolic activity upon unfavorable conditions. Many microorganisms can switch to a metabolically inactive state after water shortage, and recover once the environmental conditions become favorable again. Here, we resuscitated dormant anammox bacteria from dry terrestrial ecosystems after a resting period of >10 ka by addition of water without any other substrates. Isotopic-tracer analysis showed that water induced nitrate reduction yielding sufficient nitrite as substrate and energy for activating anammox bacteria. Subsequently, dissimilatory nitrate reduction to ammonium (DNRA) provided the substrate ammonium for anammox bacteria. The ammonium and nitrite formed were used to produce dinitrogen gas. High throughput sequencing and network analysis identified Brocadia as the dominant anammox species and a Jettenia species seemed to connect the other community members. Under global climate change, increasing precipitation and soil moisture may revive dormant anammox bacteria in arid soils and thereby impact global nitrogen and carbon cycles.
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References
Lam P, Kuypers MMM. Microbial nitrogen cycling processes in oxygen minimum zones. Annu Rev Mar Sci. 2011;3:317–45.
Zhu G, Wang S, Wang W, Wang Y, Zhou L, Jiang B, et al. Hotspots of anaerobic ammonium oxidation at land–freshwater interfaces. Nat Geosci. 2013;6:103–7.
Zhu G, Wang S, Wang Y, Wang C, Risgaard-Petersen N, Jetten MSM, et al. Anaerobic ammonia oxidation in a fertilized paddy soils. ISME J. 2011;5:1905–12.
Zhu G, Xia C, Wang S, Zhou L, Liu L, Zhao S, et al. Occurrence, activity and contribution of anammox in some freshwater extreme environments. Environ Microbiol Rep. 2015;7:961–9.
Van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Yakushevska A, Verkleij AJ, et al. Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J Struct Biol. 2008;161:401–10.
Damste JSS, Strous M, Rijpstra WIC, Hopmans EC, Geenevasen JAJ, van Duin ACT, et al. Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature. 2002;419:708–12.
Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J, et al. Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J. 2010;4:450–4.
Zhu G, Wang S, Li Y, Zhuang L, Zhao S, Wang C, et al. Microbial pathways for nitrogen loss in an upland soil. Environ Microbiol. 2018;20:1723–38.
Wang T, Zhang H, Yang F. Long-term storage and subsequent reactivation of Anammox sludge at 35 °C. Desalin Water Treat. 2016;57:24716–23.
Wang Y, Zhu G, Harhangi HR, Zhu B, Jetten MSM, Yin C, et al. Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing bacteria in a paddy soil. FEMS Microbiol Lett. 2012;336:79–88.
Zhao S, Zhuang L, Wang C, Li Y, Wang S, Zhu G. High-throughput analysis of anammox bacteria in wetland and dryland soils along the altitudinal gradient in Qinghai–Tibet plateau. Microbiol Open. 2017;7:e00556.
Magoc T, Salzberg SL. Flash: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–63.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200.
Wang Q, Quensen JF, Fish JA, Lee TK, Sun Y, Tiedje JM, et al. Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. mBio. 2013;4:e00592.
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–97.
Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71:8228–35.
Bokulich NA, Thorngate JH, Richardson PM, Mills DA. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc Natl Acad Sci USA. 2014;111:E139–48.
Vissers EW, Bodelier PLE, Muyzer G, Laanbroek HJ. A nested PCR approach for improved recovery of archaeal 16S rRNA gene fragments from freshwater samples. FEMS Microbiol Lett. 2009;298:193–8.
Zhou J, Deng Y, Luo F, He Z, Yang Y. Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. mBio. 2011;2:e00122.
Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X. Functional molecular ecological networks. mBio. 2010;1:1592–601.
Deng Y, He Z, Xu M, Qin Y, Van Nostrand JD, Wu L, et al. Elevated carbon dioxide alters the structure of soil microbial communities. Appl Environ Microbiol. 2012;78:2991–5.
Olesen JM, Bascompte J, Dupont YL, Jordano P. The modularity of pollination networks. Proc Natl Acad Sci USA. 2007;104:19891–6.
Duplessy JC, Arnold M, Maurice P, Bard E, Duprat J, Moyes J. Direct dating of the oxygen-isotope record of the last deglaciation by 14C, accelerator mass spectrometry. Nature. 1986;320:350–2.
Muller RA. Radioisotope dating with accelerators. Phys Today. 1979;32:23–30.
Hellborg R, Skog G. Accelerator mass spectrometry. Mass Spectrom Rev. 2003;70:365–72.
Risgaard-Petersen N. Anaerobic ammonium oxidation in an estuarine sediment. Aquat Microb Ecol. 2004;36:293–304.
Engström P, Dalsgaard T, Hulth S, Aller RC. Anaerobic ammonium oxidation by nitrite (anammox): implications for N2, production in coastal marine sediments. Geochim Cosmochim Acta. 2005;69:2057–65.
Thamdrup B, Dalsgaard T. Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol. 2002;68:1312–8.
Mcilvin MR, Altabet MA. Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Anal Chem. 2005;77:5589–95.
Lam P, Lavik G, Jensen MM, Vossenberg JVD, Schmid M, Woebken D, et al. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA. 2009;106:4752–7.
Layeghifard M, Hwang DM, Guttman DS. Disentangling interactions in the microbiome: a network perspective. Trends Microbiol. 2017;25:217–28.
Shnit-Orland M, Sivan A, Kushmaro A. Shewanella corallii sp nov, a marine bacterium isolated from a Red Sea coral. Int J Syst Evol Microbiol. 2010;60:2293–7.
Jones WJ, Leigh JA, Mayer F, Woese CR, Wolfe RS. Methanococcus jannaschii sp-nov, an extremely thermophilic methanogen from a submarine hydrothermal vent. Arch Microbiol. 1983;136:254–61.
Jensen MM, Lam P, Revsbech NP, Nagel B, Gaye B, Jetten MSM, et al. Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J. 2011;5:1660–70.
Fuessel J, Lam P, Lavik G, Jensen MM, Holtappels M, Guenter M, et al. Nitrite oxidation in the Namibian oxygen minimum zone. ISME J. 2012;6:1200–9.
Wood JM. Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev. 1999;63:230–62.
Orchard VA, Cook FJ. Relationship between soil respiration and soil moisture. Soil Biol Biochem. 1983;15:447–53.
Lennon JT, Jones SE. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol. 2011;9:119–30.
Dworkin J, Shah IM. Exit from dormancy in microbial organisms. Nat Rev Microbiol. 2010;8:890–6.
Antibus DE, Leff LG, Hall BL, Baeseman JL, Blackwood CB. Cultivable bacteria from ancient algal mats from the McMurdo Dry Valleys, Antarctica. Extremophiles. 2012;16:105–14.
Stephenson K, Lewis RJ. Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon. FEMS Microbiol Rev. 2005;29:281–301.
Lefelaar PA. Water movement, oxygen supply and biological processes at the aggregate scale. Geoderma. 1993;57:143–65.
Oshiki M, Satoh H, Okabe S. Ecology and physiology of anaerobic ammonium oxidizing (anammox) bacteria. Environ Microbiol. 2016;18:2784–96.
Haba RRDL, Sánchez-Porro C, Ventosa A. Taxonomy, phylogeny, and biotechnological interest of the family Halomonadaceae. Halophiles and hypersaline environments. Berlin, Heidelberg: Springer; 2011. p. 27–64.
Van Vliet S. Bacterial dormancy: how to decide when to wake up. Curr Biol. 2015;25:753–5.
Stark JM, Firestone MK. Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol. 1995;61:218–21.
Wang S, Wang W, Liu L, Zhuang L, Zhao S, Su Y, et al. Microbial nitrogen cycle hotspots in the plant-bed/ditch system of a constructed wetland with N2O mitigation. Environ Sci Technol. 2018;52:6226–36.
Ali M, Oshiki M, Awata T, Isobe K, Kimura Z, Yoshikawa H, et al. Physiological characterization of anaerobic ammonium oxidizing bacterium ‘Candidatus Jettenia caeni’. Environ Microbiol. 2015;17:2172–89.
Yan J, Haaijer SCM, Camp HJMOD, Niftrik LV, Stahl DA, Könneke M, et al. Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ Microbiol. 2012;14:3146–58.
Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart GJ, Damsté JSS. Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the arabian sea oxygen minimum zone. ISME J. 2011;5:1896.
Wang S, Radny D, Huang S, Zhuang L, Zhao S, Berg M, et al. Nitrogen loss by anaerobic ammonium oxidation in unconfined aquifer soils. Sci Rep. 2017;7:40173.
Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E, et al. Whole genome analysis of the marine bacteroidetes ‘gramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ Microbiol. 2006;8:2201–13.
Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, Passchoonen KTVD, et al. Missing lithotroph identified as new planctomycete. Nature. 1999;400:446–9.
Kelso BHL, Smith RV, Laughlin RJ, Lennox SD. Dissimilatory nitrate reduction in anaerobic sediments leading to river nitrite accumulation. Appl Environ Microbiol. 1997;63:4679–85.
Smith RV, Burns LC, Doyle RM, Lennox SD, Kelso BHL, Foy RH, et al. Free ammonia inhibition of nitrification in river sediments leading to nitrite accumulation. J Environ Qual. 1997;26:1049–55.
He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, et al. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol. 2007;9:2364–74.
Wang S, Wang Y, Feng X, Zhai L, Zhu G. Quantitative analyses of ammonia-oxidizing archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Appl Microbiol Biotechnol. 2011;90:779–87.
Zhou L, Wang S, Zou Y, Xia C, Zhu G. Species, abundance and function of ammonia-oxidizing archaea in inland waters across China. Sci Rep. 2015;5:15969.
Yin S, Chen D, Chen L, Edis R. Dissimilatory nitrate reduction to ammonium and responsible microorganisms in two Chinese and Australian paddy soils. Soil Biol Biochem. 2002;34:1131–7.
Jones ZL, Jasper JT, Sedlak DL, Sharpa JO. Sulfide-induced dissimilatory nitrate reduction to ammonium supports anaerobic ammonium oxidation (Anammox) in an open-water unit process wetland. Appl Environ Microbiol. 2017;83:e00782.
Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA. 2005;102:6478–83.
Acknowledgements
This research was financially supported by the National Natural Science Foundation of China (Nos. 41322012, 41671471, and 91851204), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020303), Local Innovative and Research Teams Project of Guangdong Pearl River Talents Program (2017BT01Z176), National Key R&D Program (2016YFA0602303), and a special fund from the Key Laboratory of Drinking Water Science and Technology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (15Z07KLDWST and 16Z03KLDWST). The author Guibing Zhu gratefully acknowledges the Program of the Youth Innovation Promotion Association (CAS). Mike Jetten was supported by erc ag 232937 anammox, erc ag ecomom 339880, and siam 024002002. LS acknowledges support by the German Research Foundation (Schw554/25).
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Zhu, G., Wang, S., Wang, C. et al. Resuscitation of anammox bacteria after >10,000 years of dormancy. ISME J 13, 1098–1109 (2019). https://doi.org/10.1038/s41396-018-0316-5
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DOI: https://doi.org/10.1038/s41396-018-0316-5
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