Community diversity and distribution of ammonia-oxidizing archaea in marsh wetlands in the black soil zone in North-east China

Highlights

AOA amoA genes in the soils of the two wetlands affiliated with three lineages.

The main drivers of AOA community were pH and total organic carbon and ammonium.

The soil characteristics rather than the vegetation control the AOA community.

Abstract

Since its first detection, ammonia-oxidizing archaea (AOA) have been proven to be ubiquitous in aquatic and terrestrial ecosystems. In this study, two freshwater marsh wetlands- the Honghe wetland and Qixinghe wetland – in the black soil zone in North-east China were chosen to investigate the AOA community diversity and distribution in wetland soils with different vegetation and depth. In the Honghe wetland, two sampling locations were chosen as the dominant plant transited from Deyeuxia to Carex. In the Qixinghe wetland, one sample location that was dominated by Deyeuxia was chosen. Samples of each location were collected from three different depths, and Illumina MiSeq platform was used to generate the AOA amoA gene archive. The results showed that the AOA amoA genes in the soils of the two wetlands were affiliated with three lineages: Nitrososphaera, Nitrosotalea, and Nitrosopumilus clusters. The different dominant status of these AOA lineages indicated their differences in adapting to acidic habitat, oxygenic/hypoxic alternation, organic matter, and other environmental factors, suggesting high diversity among AOA in marsh soils. The main driver of the AOA community was pH, along with organic carbon and ammonium nitrogen, which also played an important role combined with many other environmental factors. Thus, soil physiochemical characteristics, rather than vegetation, were the main cause of AOA community diversity in the wetlands in the black soil zone in China.

Graphical abstract

Keywords

Ammonia-oxidizing archaea / amoA gene / Freshwater marsh / Diversity / Distribution

References

[1] Alves R J E, Minh B Q, Urich T, von Haeseler A, Schleper C (2018). Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nature Communications, 9(1): 1517–1533

[2] Auguet J C, Triadó-Margarit X, Nomokonova N, Camarero L, Casamayor E O (2012). Vertical segregation and phylogenetic characterization of ammonia-oxidizing Archaea in a deep oligotrophic lake. ISME J, 6(9): 1786–1797

[3] Bertagnolli A D, Ulloa O (2017). Hydrography shapes community composition and diversity of amoA-containing Thaumarchaeota in the coastal waters off central Chile. Environmental Microbiology Reports, 9(6): 717–728

[4] Biller S J, Mosier A C, Wells G F, Francis C A (2012). Global biodiversity of aquatic ammonia-oxidizing archaea is partitioned by habitat. Frontiers in Microbiology, 3: 252

[5] Blainey P C, Mosier A C, Potanina A, Francis C A, Quake S R (2011). Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One, 6(2): e16626

[6] Boratyn G M, Camacho C, Cooper P S, Coulouris G, Fong A, Ma N, Madden T L, Matten W T, McGinnis S D, Merezhuk Y, Raytselis Y, Sayers E W, Tao T, Ye J, Zaretskaya I (2013). BLAST: A more efficient report with usability improvements. Nucleic Acids Research, 41(W1): W29-W33

[7] Bouskill N J, Eveillard D, Chien D, Jayakumar A, Ward B B (2012). Environmental factors determining ammonia-oxidizing organism distribution and diversity in marine environments. Environmental Microbiology, 14(3): 714–729

[8] Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008). Mesophilic Crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nature Reviews Microbiology, 6(3): 245–252

[9] Brochier-Armanet C, Gribaldo S, Forterre P (2012). Spotlight on the Thaumarchaeota. ISME J, 6(2): 227–230

[10] Caffrey J M, Bano N, Kalanetra K, Hollibaugh J T (2007). Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J, 1(7): 660–662

[11] Chen C H, Gao D W, Tao Y (2013). Diversity and distribution of ammonia-oxidizing Archaea in the seasonally frozen soils in Northeastern China. Applied Microbiology and Biotechnology, 97(14): 6571–6579

[12] de la Torre J R, Walker C B, Ingalls A E, Könneke M, Stahl D A (2008). Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environmental Microbiology, 10(3): 810–818

[13] Fernàndez-Guerra A, Casamayor E O (2012). Habitat-associated phylogenetic community patterns of microbial ammonia oxidizers. PLoS One, 7(10): e47330

[14] Fish J A, Chai B, Wang Q, Sun Y, Brown C T, Tiedje J M, Cole J R (2013). FunGene: The functional gene pipeline and repository. Frontiers in Microbiology, 4: 291

[15] Francis C A, Roberts K J, Beman J M, Santoro A E, Oakley B B (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America, 102(41): 14683–14688

[16] Fu L, Niu B, Zhu Z, Wu S, Li W (2012). CD-HIT: Accelerated for clustering the next-generation sequencing data. Bioinformatics (Oxford, England), 28(23): 3150–3152

[17] Gao D, Liu F, Xie Y, Liang H (2018). Temporal and spatial distribution of ammonia-oxidizing organisms of two types of wetlands in Northeast China. Applied Microbiology and Biotechnology, 102(16): 7195–7205

[18] Hallam S J, Konstantinidis K T, Putnam N, Schleper C, Watanabe Y, Sugahara J, Preston C, de la Torre J, Richardson P M, DeLong E F (2006). Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proceedings of the National Academy of Sciences of the United States of America, 103(48): 18296–18301

[19] Hatzenpichler R, Lebedeva E V, Spieck E, Stoecker K, Richter A, Daims H, Wagner M (2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Sciences of the United States of America, 105(6): 2134–2139

[20] Hu H W, Zhang L M, Dai Y, Di H J, He J Z (2013). pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. Journal of Soils and Sediments, 13(8): 1439–1449

[21] Jetten M S (2008). The microbial nitrogen cycle. Environmental Microbiology, 10(11): 2903–2909

[22] Könneke M, Bernhard A E, de la Torre J R, Walker C B, Waterbury J B, Stahl D A (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437(7058): 543–546

[23] Kuypers M M M, Marchant H K, Kartal B (2018). The microbial nitrogen-cycling network. Nature Reviews Microbiology, 16(5): 263–276

[24] Lebedeva E V, Hatzenpichler R, Pelletier E, Schuster N, Hauzmayer S, Bulaev A, Grigor’eva N V, Galushko A, Schmid M, Palatinszky M, Le Paslier D, Daims H, Wagner M (2013). Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon “Ca. Nitrosotenuis uzonensis” representing a clade globally distributed in thermal habitats. PLoS One, 8(11): e80835

[25] Lehtovirta-Morley L E, Stoecker K, Vilcinskas A, Prosser J I, Nicol G W (2011). Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proceedings of the National Academy of Sciences of the United States of America, 108(38): 15892–15897

[26] Letunic I, Bork P (2016). Interactive tree of life (iTOL) v3: An online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Research, 44(W1): W242-W245

[27] Li M, Wei G, Shi W, Sun Z, Li H, Wang X, Gao Z (2018). Distinct distribution patterns of ammonia-oxidizing archaea and bacteria in sediment and water column of the Yellow River estuary. Scientific Reports, 8(1): 1584

[28] Li Y C, Liu B R, Li S H, Qin H, Fu W J, Xu Q F (2014). Shift in abundance and structure of soil ammonia-oxidizing bacteria and archaea communities associated with four typical forest vegetations in subtropical region. Journal of Soils and Sediments, 14(9): 1577–1586

[29] Liu J, Yu Z, Yao Q, Sui Y, Shi Y, Chu H, Tang C, Franks A E, Jin J, Liu X, Wang G (2018). Ammonia-oxidizing archaea show more distinct biogeographic distribution patterns than ammonia-oxidizing bacteria across the black soil zone of Northeast China. Frontiers in Microbiology, 9: 171

[30] Liu S, Hu B, He Z, Zhang B, Tian G, Zheng P, Fang F (2015). Ammonia-oxidizing archaea have better adaptability in oxygenated/hypoxic alternant conditions compared to ammonia-oxidizing bacteria. Applied Microbiology and Biotechnology, 99(20): 8587–8596

[31] Liu Y, Zhang J, Zhang X, Xie S (2014). Depth-related changes of sediment ammonia-oxidizing microorganisms in a high-altitude freshwater wetland. Applied Microbiology and Biotechnology, 98(12): 5697–5707

[32] Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart A W, Gross O, Grumann S, Hermann S, Jost R, KönigA, Liss T, Lüβmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, LudwigT, Bode A, Schleifer K H (2004). ARB: A software environment for sequence data. Nucleic Acids Research, 32(4): 1363–1371

[33] Ma B, Dai Z, Wang H, Dsouza M, Liu X, He Y, Wu J, Rodrigues J L M, Gilbert J A, Brookes P C, Xu J (2017). Distinct biogeographic patterns for archaea, bacteria, and fungi along the vegetation gradient at the continental scale in eastern China. mSystems, 2(1): e00174-16

[34] Mao D H, Wang Z M, Luo L, Ren C Y, Jia M M (2016). Monitoring the evolution of wetland ecosystem pattern in northeast China from 1990 to 2013 based on remote sensing. Journal of Natural Resources, 31(8): 1253–1263

[35] Martens-Habbena W, Berube P M, Urakawa H, de la Torre J R, Stahl D A (2009). Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature, 461(7266): 976–979

[36] Mehrshad M, Amoozegar M A, Ghai R, Shahzadeh Fazeli S A, Rodriguez-Valera F (2016). Genome reconstruction from metagenomic data sets reveals novel microbes in the brackish waters of the Caspian Sea. Applied and Environmental Microbiology, 82(5): 1599–1612

[37] Mukhtar H, Lin Y, Anthony J (2017). Ammonia oxidizing archaea and bacteria in east Asian paddy soils: A mini review. Environments, 4(4)86‒75

[38] Newell S E, Fawcett S E, Ward B B (2013). Depth distribution of ammonia oxidation rates and ammonia-oxidizer community composition in the Sargasso Sea. Limnology and Oceanography, 58(4): 1491–1500

[39] Nicol G W, Schleper C (2006). Ammonia-oxidising Crenarchaeota: Important players in the nitrogen cycle? Trends in Microbiology, 14(5): 207–212

[40] Niu Z G, Gong P, Cheng X, Guo J H, Wang L, Huang H B, Shen S Q, Wu Y Z, Wang X F, Wang X W, Ying Q, Liang L, Zhang L N, Wang L, Yao Q, Yang Z Z, Guo Z Q, Dai Y J (2009). Geographical characteristics of China’s wetlands derived from remotely sensed data. Science in China. Series D, Earth Sciences, 52(6): 723–738

[41] Pan H, Xie K X, Zhang Q C, Jia Z J, Xu J M, Di H J, Li Y (2018). Archaea and bacteria respectively dominate nitrification in lightly and heavily grazed soil in a grassland system. Biology and Fertility of Soils, 54(1): 41–54

[42] Peralta A L, Matthews J W, Kent A D (2014). Habitat specialization along a wetland moisture gradient differs between ammonia-oxidizing and denitrifying microorganisms. Microbial Ecology, 68(2): 339–350

[43] Pester M, Rattei T, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012). amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environmental Microbiology, 14(2): 525–539

[44] Pester M, Schleper C, Wagner M (2011). The Thaumarchaeota: An emerging view of their phylogeny and ecophysiology. Current Opinion in Microbiology, 14(3): 300–306

[45] Pierre S, Hewson I, Sparks J P, Litton C M, Giardina C, Groffman P M, Fahey T J (2017). Ammonia oxidizer populations vary with nitrogen cycling across a tropical montane mean annual temperature gradient. Ecology, 98(7): 1896–1907

[46] Prosser J I, Nicol G W (2008). Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environmental Microbiology, 10(11): 2931–2941

[47] Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016). VSEARCH: A versatile open source tool for metagenomics. PeerJ, 4: e2584

[48] Sauder L A, Albertsen M, Engel K, Schwarz J, Nielsen P H, Wagner M, Neufeld J D (2017). Cultivation and characterization of Candidatus Nitrosocosmicus exaquare, an ammonia-oxidizing archaeon from a municipal wastewater treatment system. ISME J, 11(5): 1142–1157

[49] Sauder L A, Engel K, Lo C C, Chain P, Neufeld J D (2018). “Candidatus Nitrosotenuis aquarius,” an ammonia-oxidizing archaeon from a freshwater aquarium biofilter. Applied and Environmental Microbiology, 84(19): e01430-18

[50] Schleper C, Jurgens G, Jonuscheit M (2005). Genomic studies of uncultivated archaea. Nature Reviews Microbiology, 3(6): 479–488

[51] Schloss P D, Westcott S L, Ryabin T, Hall J R, Hartmann M, Hollister E B, Lesniewski R A, Oakley B B, Parks D H, Robinson C J, Sahl J W, Stres B, Thallinger G G, Van Horn D J, Weber C F (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23): 7537–7541

[52] Shen J P, Zhang L M, Di H J, He J Z (2012). A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Frontiers in Microbiology, 3: 296

[53] Stempfhuber B, Engel M, Fischer D, Neskovic-Prit G, Wubet T, Schöning I, Gubry-Rangin C, Kublik S, Schloter-Hai B, Rattei T, Welzl G, Nicol G W, Schrumpf M, Buscot F, Prosser J I, Schloter M (2015). pH as a driver for ammonia-oxidizing archaea in forest soils. Microbial Ecology, 69(4): 879–883

[54] Tao R, Wakelin S A, Liang Y C, Chu G X (2017). Response of ammonia-oxidizing archaea and bacteria in calcareous soil to mineral and organic fertilizer application and their relative contribution to nitrification. Soil Biology & Biochemistry, 114: 20–30

[55] Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011). Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proceedings of the National Academy of Sciences of the United States of America, 108(20): 8420–8425

[56] Valentine D L (2007). Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nature Reviews Microbiology, 5(4): 316–323

[57] Wang Z, Wang Z, Huang C, Pei Y (2014). Vertical distribution of ammonia-oxidizing archaea (AOA) in the hyporheic zone of a eutrophic river in North China. World Journal of Microbiology & Biotechnology, 30(4): 1335–1346

[58] Ward B B, Jensen M M (2014). The microbial nitrogen cycle. Frontiers in Microbiology, 5: 553

[59] Wu Y C, Lu L, Wang B Z, Lin X G, Zhu J G, Cai Z C, Yan X Y, Jia Z J (2011). Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather thanarchaea in a paddy soil. Soil Science Society of America Journal, 75(4): 1431–1439

[60] Xi R, Long X E, Huang S, Yao H (2017). pH rather than nitrification and urease inhibitors determines the community of ammonia oxidizers in a vegetable soil. AMB Express, 7(1): 129

[61] Zhang Q, Tang F, Zhou Y, Xu J, Chen H, Wang M, Laanbroek H J (2015). Shifts in the pelagic ammonia-oxidizing microbial communities along the eutrophic estuary of Yong River in Ningbo City, China. Frontiers in Microbiology, 6: 1180

[62] Zhou J, Bruns M A, Tiedje J M (1996). DNA recovery from soils of diverse composition. Applied and Environmental Microbiology, 62(2): 316–322

[63] Zhou L, Wang S, Zou Y, Xia C, Zhu G (2015). Species, abundance and function of ammonia-oxidizing archaea in inland waters across China. Scientific Reports, 5(1): 15969

[64] Zhou Z, Zhang G X, Xu Y B, Gu J D (2018). Successive transitory distribution of Thaumarchaeota and partitioned distribution of Bathyarchaeota from the Pearl River estuary to the northern South China Sea. Applied Microbiology and Biotechnology, 102(18): 8035–8048

Acknowledgments

This research was funded by the National Natural Science Foundation of China (Grang Nos. 31870471 and 31470543) and the State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (No. 2014DX07). We thank for the Administration of Honghe National Natural Reservation and the Administration of Qixinghe National Natural Reservation that have provided lots of help on the sites choosing and sampling. Yunlong Yao, PhD., Xiaolong Wang, PhD., and Lixin Sui gave great help on the field experiments. Yue Xie provided the sequencing and chemical analyzing data of Sanjiang wetland and Zhalong wetland for the statistical comparison.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-019-1146-z and is accessible for authorized users.

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