Carbon-nitrogen biogeochemical cycle processes driven by ammonia-oxidizing archaea in marine environment

doi:10.7523/j.issn.2095-6134.2020.04.001

Abstract

Abstract: Ammonia-oxidizing archaea (AOA), one kind of the most abundant prokaryotes in the seawater, is widely distributed in the marine environment. As the dominant microorganism of ammonia oxidation in the ocean, AOA fixes carbon with chemoautotroph under oligotrophic conditions and plays an important role in marine nitrogen and carbon cycles. This autotrophic carbon sequestration driven by AOA ammonia oxidation process is an important energy source in deep sea, which is significant for understanding the imbalance between organic carbon input and microbial energy demand in deep sea. At the same time, the energy from this autotrophic microorganism fuels the deep-sea ecological system. In this paper, we review the diversity distribution of AOA and the process and function of AOA in biogeochemical cycles of carbon and nitrogen in order to provide information for the researchers in this field.

Key words: ammonia-oxidizing archaea, ammonia-oxidizing process, chemoautotrophic carbon-fixing, biogeochemical cycle, marine water column

CLC Number:

Q938.8

HONG Yiguo, HE Xiang, WU Jiapeng, LIU Xiaohan. Carbon-nitrogen biogeochemical cycle processes driven by ammonia-oxidizing archaea in marine environment[J]. , 2020, 37(4): 433-441.

References

[1] Canfield D E, Glazer A N, Falkowski P G. The evolution and future of earth's nitrogen cycle[J]. Science, 2010, 330(6001):192-196.
[2] Daims H, Lebedeva E V, Pjevac P, et al. Complete nitrification by Nitrospira bacteria[J]. Nature, 2015, 528(7583):504-509.
[3] Francis C A, Beman J M, Kuypers M M M. New processes and players in the nitrogen cycle:the microbial ecology of anaerobic and archaeal ammonia oxidation[J]. The ISME Journal, 2007, 1(1):19-27.
[4] Klotz M G, Stein L Y. Nitrifier genomics and evolution of the nitrogen cycle[J]. FEMS Microbiology Letters, 2008, 278(2):146-156.
[5] Ward B, Capone D, Zehr J. What's new in the nitrogen cycle?[J]. Oceanography, 2007, 20(2):101-109.
[6] Troelstra S R, Wagenaar R, Boer W D. Nitrification in Dutch heathland soils:I. General soil characteristics and nitrification in undisturbed soil cores[J]. Plant and Soil, 1990, 127(2):179-192.
[7] Winogradsky S. Recherches sur les organisms de la nitrification[J]. Annales de L Institut Pasteur. Microbiology, 1890, 4:213-231.
[8] Bennett K, Sadler N C, Wright A T, et al. Activity-based protein profiling of ammonia monooxygenase in Nitrosomonas europaea[J]. Applied and Environmental Microbiology, 2016, 82(8):2270-2279.
[9] Chain P, Lamerdin J, Larimer F, et al. Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea[J]. Journal of Bacteriology, 2003, 185(9):2759-2773.
[10] Kozlowski J A, Price J, Stein L Y. Revision of N₂O-producing pathways in the ammonia-oxidizing bacterium Nitrosomonas europaea ATCC 19718[J]. Applied and Environmental Microbiology, 2014, 80(16):4930-4935.
[11] Rotthauwe J H, Witzel K P, Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker:molecular fine-scale analysis of natural ammonia-oxidizing populations[J]. Applied and Environmental Microbiology, 1997, 63(12):4704-4712.
[12] Campbell M A, Chain P S G, Dang H, et al. Nitrosococcus watsonii sp. Nov., a new species of marine obligate ammonia-oxidizing bacteria that is not omnipresent in the world's oceans:calls to validate the names ‘Nitrosococcus halophilus’ and ‘Nitrosomonas mobilis’[J]. FEMS Microbiology Ecology, 2010, 76(1):39-48.
[13] Monteiro M, Séneca J, Magalhães C. The history of aerobic ammonia oxidizers:from the first discoveries to today[J]. Journal of Microbiology, 2014, 52(7):537-547.
[14] Purkhold U, PommereningRöser A, Juretschko S, et al. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis:implications for molecular diversity surveys[J]. Applied and Environmental Microbiology, 2000, 66(12):5368-5382.
[15] Urakawa H, Garcia J C, Nielsen J L, et al. Nitrosospira lacus sp. Nov., a psychrotolerant, ammonia-oxidizing bacterium from sandy lake sediment[J]. International Journal of Systematic and Evolutionary Microbiology, 2015, 65(1):242-250.
[16] Lin W, Kent L C, Hongyue D, et al. D1FHS, the type strain of the ammonia-oxidizing bacterium Nitrosococcus wardiae spec. Nov.:enrichment, isolation, phylogenetic, and growth physiological characterization[J]. Frontiers in Microbiology, 2016, 7(512):75.
[17] Ward B B, O'Mullan G D. Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing γ-proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes[J]. Applied and Environmental Microbiology, 2002, 68(8):4153-4157.
[18] Jordan F L, Cantera J J L, Fenn M E, et al. Autotrophic ammonia-oxidizing bacteria contribute minimally to nitrification in a nitrogen-impacted forested ecosystem[J]. Applied and Environmental Microbiology, 2005, 71(1):197-206.
[19] Venter J C, Remington K, Heidelberg J F, et al. Environmental genome shotgun sequencing of the Sargasso Sea[J]. Science, 2004, 304(5667):66-74.
[20] Schleper C, Jurgens G, Jonuscheit M. Genomic studies of uncultivated archaea[J]. Nature Reviews Microbiology, 2005, 3(6):479-488.
[21] Treusch A H, Leininger S, Kletzin A, et al. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic Crenarchaeota in nitrogen cycling[J]. Environmental Microbiology, 2005, 7(12):1985-1995.
[22] Könneke M, Bernhard A E, de la Torre, José R, et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon[J]. Nature, 2005, 437(7058):543-546.
[23] Mincer T J, Church M J, Taylor L T, et al. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre[J]. Environmental microbiology, 2007, 9(5):1162-1175.
[24] Wuchter C, Abbas B, Coolen M J L, et al. Archaeal nitrification in the ocean[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(33):12317-12322.
[25] Martens-Habbena W, Berube P M, Urakawa H, et al. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria[J]. Nature, 2009, 461(7266):976-979.
[26] DeLong E F. Oceans of archaea[J]. ASM News, 2003, 69(10):503-511.
[27] Delong E F. Everything in moderation:archaea as ‘non-extremophiles’[J]. Current Opinion in Genetics & Development, 1998, 8(6):649-654.
[28] Robertson C E, Harris J K, Spear J R, et al. Phylogenetic diversity and ecology of environmental archaea[J]. Current Opinion in Microbiology, 2005, 8(6):638-642.
[29] Brochier-Armanet C, Boussau B, Gribaldo S, et al. Mesophilic Crenarchaeota:proposal for a third archaeal phylum, the Thaumarchaeota[J]. Nature Reviews Microbiology, 2008, 6(3):245-252.
[30] 张丽梅, 贺纪正. 一个新的古菌类群:奇古菌门(Thaumarchaeota)[J]. 微生物学报, 2012, 52(4):411-421.
[31] Biller S J, Mosier A C, Wells G F, et al. Global biodiversity of aquatic ammonia-oxidizing archaea is partitioned by habitat[J]. Frontiers in Microbiology, 2012, 3:252.
[32] Pester M, Rattei T, Flechl S, et al. amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions[J]. Environmental Microbiology, 2012, 14(2):525-539.
[33] Arp D J, Chain P S, Klotz M G. The impact of genome analyses on our understanding of ammonia-oxidizing bacteria[J]. Annual Review Microbiology, 2007, 61(1):503.
[34] Nicol G W, Schleper C. Ammonia-oxidizing Crenarchaeota:important players in the nitrogen cycle?[J]. Trends in Microbiology, 2006, 14(5):207-212.
[35] Glass J B, Orphan V J. Trace metal requirements for microbial enzymes involved in the production and consumption of methane and nitrous oxide[J]. Frontiers in Microbiology, 2012, 3:61.
[36] Walker C B, de la Torre J R, Klotz M G, et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea[J]. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(19):8818-8823.
[37] Stahl D A, de la Torre J R. Physiology and diversity of ammonia-oxidizing archaea[J]. Annual Review of Microbiol, 2012, 66(1):83-101.
[38] Vajrala N, Martens-Habbena W, Sayavedra-Soto L A, et al. Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(3):1006-1011.
[39] Fuhrman J A, McCallum K, Davis A A. Novel major archaebacterial group from marine plankton[J]. Nature, 1992, 356(6365):148-149.
[40] Delong E F. Archaea in coastal marine environments[J]. Proceedings of the National Academy of Sciences of the United States of America, 1992, 89(12):5685-5689.
[41] Karner M B, Delong E F, Karl D M. Archaeal dominance in the mesopelagic zone of the Pacific ocean[J]. Nature, 2001, 409(6819):507-510.
[42] Teira E, Lebaron P, van Aken H, et al. Distribution and activity of bacteria and archaea in the deep water masses of the North Atlantic[J]. Limnology and Oceanography, 2006, 51(5):2131-2144.
[43] Teira E, Reinthaler T, Pernthaler A, et al. Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and archaea in the deep ocean[J]. Applied and Environmental Microbiology, 2004, 70(7):4411-4414.
[44] Francis C A, Roberts K J, Beman J M, et al. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(41):14683-14688.
[45] Baker B J, Lesniewski R A, Dick G J. Genome-enabled transcriptomics reveals archaeal populations that drive nitrification in a deep-sea hydrothermal plume[J]. The ISME Journal, 2012, 6(12):2269-2279.
[46] Hollibaugh J T, Gifford S, Sharma S, et al. Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage[J]. The ISME Journal, 2010, 5(5):866-878.
[47] Stewart F J, Ulloa O, DeLong E F. Microbial metatranscriptomics in a permanent marine oxygen minimum zone[J]. Environmental Microbiology, 2012, 14(1):23-40.
[48] Kelly D. Bioenergetics of chemolithotrophic bacteria[M]. London:InCompanion to Microbiology, 1978:363-386.
[49] Blainey P C, Mosier A C, Potanina A, et al. Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis[J]. PLOS ONE, 2011, 6(2):e16626.
[50] Hallam S J, Konstantinidis K T, Putuam N, et al. Genomic analysis of the uncultivated marine crenarchaeote cenarchaeum symbiosum[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(48):18296-18301.
[51] Spang A, Poehlein A, Offre P, et al. The genome of the ammonia-oxidizing Candidatus nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations[J]. Environmental Microbiology, 2012, 14(12):3122.
[52] Tourna M, Stieglmeier M, Spang A, et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(20):8420-8425.
[53] Könneke M, Schubert D M, Brown P C, et al. Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO₂ fixation[J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(22):8239-8244.
[54] Bergauer K, Sintes E, van Bleijswijk J, et al. Abundance and distribution of archaeal acetyl-CoA/propionyl-CoA carboxylase genes indicative for putatively chemoautotrophic archaea in the tropical Atlantic's interior[J]. FEMS Microbiology Ecology, 2013, 84(3):461-473.
[55] Hu A, Jiao N, Zhang C L. Community structure and function of planktonic Crenarchaeota: changes with depth in the South China Sea[J]. Microbial Ecology, 2011a, 62(3):549-563.
[56] Hu A, Jiao N, Zhang R, et al. Niche partitioning of marine group Crenarchaeota in the euphotic and upper mesopelagic zones of the east china sea[J]. Applied and Environmental Microbiology, 2011b, 77(21):7469-7478.
[57] Song Z Q, Wang L, Wang F P, et al. Abundance and diversity of archaeal accA gene in hot springs in Yunnan Province, China[J]. Extremophiles, 2013, 17(5):871-879.
[58] Yakimov M M, Cono V L, Denaro R. A first insight into the occurrence and expression of functional amoA and accA genes of autotrophic and ammonia-oxidizing bathypelagic Crenarchaeota, of Tyrrhenian Sea[J]. Deep Sea Research Part II:Topical Studies in Oceanography, 2009, 56(11/12):748-754.
[59] Yakimov M M, Cono V L, Smedile F, et al. Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea)[J]. The ISME Journal, 2011, 5(6):945-961.
[60] P A del Giorgio, Duarte C M. Respiration in the open ocean[J]. Nature, 2002, 420(6914):379-384.
[61] Carlson C A, Ducklow H W, Michaels A F. Annual flux of dissolved organic carbon from the euphotic zone in the Northwestern Sargasso Sea[J]. Nature, 1994, 371(6496):405-408.
[62] Reinthaler T, van Aken H, Veth C, et al. Prokaryotic respiration and production in the meso-and bathypelagic realm of the eastern and western North Atlantic Basin[J]. Limnology and Oceanography, 2006, 51(3):1262-1273.
[63] Karl D M, Knauer G A, Martin J H, et al. Bacterial chemolithotrophy in the ocean is associated with sinking particles[J]. Nature, 1984, 309(5963):54-56.
[64] Middelburg J J. Chemoautotrophy in the ocean[J]. Geophysical Research Letters, 2011, 38(24):L26404.
[65] Ingalls A E, Shah S R, Hansman R L, et al. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(17):6442-6447.
[66] Hansman R L, Griffin S, Watson J T, et al. The radiocarbon signature of microorganisms in the mesopelagic ocean[J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(16):6513-6518.
[67] Herndl G J, Reinthaler T, Teira E, et al. Contribution of archaea to total prokaryotic production in the deep Atlantic ocean[J]. Applied Environmental Microbiology, 2005, 71(5):2303-2309.
[68] Tetu S G, Breakwell K, Elbourne L D H, et al. Life in the dark:metagenomic evidence that a microbial slime community is driven by inorganic nitrogen metabolism[J]. The ISME Journal, 2013, 7(6):1227-1236.
[69] Reinthaler T, van Aken H M, Herndl G J. Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic Basin[J]. Deep Sea Research Part II:Topical Studies in Oceanography, 2010, 57(16):1572-1580.
[70] Jiao N, Herndl G J, Hansell D A, et al. Microbial production of recalcitrant dissolved organic matter:long-term carbon storage in the global ocean[J]. Nature Reviews Microbiology, 2010, 8(8):593-599.
[71] Jiao N, Herndl G J, Hansell D A, et al. The microbial carbon pump and the oceanic recalcitrant dissolved organic matter pool[J]. Nature Reviews Microbiology, 2011, 9(7):555.