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A Single Thaumarchaeon Drives Nitrification in Deep Oligotrophic

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A Single Thaumarchaeon Drives Nitrification in Deep Oligotrophic Environmental Microbiology (2020) 22(1), 212–228 doi:10.1111/1462-2920.14840 A single Thaumarchaeon drives nitrification in deep oligotrophic Lake Constance Janina Herber,1 Franziska Klotz,1 typically two orders of magnitude less abundant and Benjamin Frommeyer,1 Severin Weis,2 Dietmar Straile,3 completely ammonia-oxidizing (comammox) bacteria Allison Kolar,4 Johannes Sikorski,5 Markus Egert,2 were not detected. Both, 16S rRNA gene and amoA Michael Dannenmann4 and Michael Pester 1,5,6* (encoding ammonia monooxygenase subunit B) ana- 1Department of Biology, University of Konstanz, lyses identified only one major species-level opera- Universitätsstrasse 10, Constance 78457, Germany. tional taxonomic unit (OTU) of Thaumarchaeota (99% 2Faculty of Medical and Life Sciences, Institute of of all ammonia oxidizers in the hypolimnion), which Precision Medicine, Furtwangen University, Jakob- was affiliated to Nitrosopumilus spp. The relative abun- Kienzle-Str. 17, Villingen-Schwenningen 78054, dance distribution of the single Thaumarchaeon Germany. strongly correlated to an equally abundant Chloroflexi 3Limnological Institute, University of Konstanz, clade CL500-11 OTU and a Nitrospira OTU that was one Mainaustraße 252, Constance 78464, Germany. order of magnitude less abundant. The latter domi- 4Karlsruhe Institute of Technology, Institute for nated among recognized nitrite oxidizers. This fi Meteorology and Climate Research, Atmospheric extremely low diversity of nitri ers shows how vulnera- fi Environmental Research (IMK-IFU), Kreuzeckbahnstr. ble the ecosystem process of nitri cation may be in ’ 19, 82467 Garmisch-Partenkirchen, Germany. Lake Constance as Central Europe s third largest lake. 5Department of Microorganisms, Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Introduction Cultures, Inhoffenstr. 7B, 38124 Braunschweig, Microbially driven ammonia oxidation to nitrite is the rate Germany. limiting step in nitrification and as such an important part 6Technical University of Braunschweig, Institute for of the global nitrogen cycle (Jetten, 2008). Although nitri- Microbiology, Spielmannstrasse 7, 38106 fication does not directly change the inventory of inor- Braunschweig, Germany. ganic N in freshwater ecosystems, it constitutes the only known biological source of nitrate and as such a critical Summary link between mineralization of organic N and its eventual loss as N by denitrification or anaerobic ammonia oxida- Ammonia released during organic matter mineraliza- 2 tion to the atmosphere (Jetten, 2008). The process of tion is converted during nitrification to nitrate. We followed spatiotemporal dynamics of the nitrifying ammonia oxidation is known to be catalysed by three dif- microbial community in deep oligotrophic Lake Con- ferent microbial guilds. Two of these guilds, the ammonia- stance. Depth-dependent decrease of total ammonium oxidizing bacteria (AOB; Bock and Wagner, 2013) and (0.01–0.84 μM) indicated the hypolimnion as the major ammonia-oxidizing archaea (AOA; Pester et al., 2011; place of nitrification with 15N-isotope dilution measure- Alves et al., 2018) oxidize ammonia to nitrite and depend ments indicating a threefold daily turnover of on nitrite oxidizing bacteria (NOB; Daims et al., 2016) to hypolimnetic total ammonium. This was mirrored by a complete nitrification by further oxidation of nitrite to strong increase of ammonia-oxidizing Thaumarchaeota nitrate. The third guild oxidizes ammonia directly to nitrate towards the hypolimnion (13%–21% of bacter- and is therefore referred to as complete ammonia oxi- ioplankton) throughout spring to autumn as revealed dizers (comammox; Daims et al., 2015; van Kessel et al., by amplicon sequencing and quantitative polymerase 2015). Most AOB belong to a monophyletic branch within chain reaction. Ammonia-oxidizing bacteria were the Betaproteobacteria represented by the genera Nitrosomonas and Nitrosospira, with the latter including the former genera Nitrosolobus and Nitrosovibrio,while Received 11 March, 2019; revised 30 August, 2019; accepted 30 August, 2019. *For correspondence. E-mail michael.pester@dsmz. the genus Nitrosococcus constitutes a separate branch de; Tel. (+49) 531 2616 237; Fax: (+49) 531 2616 418. within the Gammaproteobacteria (Head et al., 1993; Bock © 2019 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. The nitrifying community in a deep lake 213 and Wagner, 2013). Among the AOA, four major lineages 2013; Vissers et al., 2013a; Mukherjee et al., 2016; Oka- represented by the two orders Nitrosopumilales and zaki and Nakano, 2016; Yang et al., 2016). In snapshot Nitrososphaerales and the two deep-branching Candidatus analyses of oligotrophic lakes, AOA typically outnumbered genera Nitrosotalea and Nitrosocaldus constitute together a AOB and constituted preferentially in the deep oxygenated major part of the diversity within the phylum Thaumarchaeota hypolimnion large bacterioplankton populations (Urbach (Stieglmeier et al., 2014b; Lehtovirta-Morley et al., 2016; Qin et al., 2001; Callieri et al., 2016; Mukherjee et al., 2016). et al., 2017). Based on a phylogenomic framework, it was Whether this picture changes during the yearly phyto- recently proposed to re-integrate the Thaumarchaeota into plankton succession of lakes and how comammox contrib- the phylum Crenarchaeota (Parks et al., 2018), which awaits ute to this functional group of microorganisms is not clear validation by the International Committee on Systematics of yet. Here, we followed the yearly bacterioplankton cycle of Prokaryotes. The comammox bacteria are currently deep oligotrophic Lake Constance to identify spatiotempo- described for the genus Nitrospira (phylum Nitrospirae)only ral dynamics of the nitrifying microbial community and link (Daims et al., 2015; van Kessel et al., 2015), which is next to this to nitrification activity. Nitrospinae, Chloroflexi and Alpha-, Beta- and Gamma- proteobacteria one of the six phylogenetic lineages that har- bours also strict NOB (Daims et al., 2016). Results The presence and relative abundance of AOA and AOB Active nitrification in the hypolimnion of upper Lake have been extensively studied over the past decade in soils Constance (e.g., Leininger et al., 2006; Prosser and Nicol, 2008; Pester fi et al., 2012; Hink et al., 2018), the ocean (e.g., Wuchter Depth pro les of total ammonium and nitrate as the primary fi et al., 2006; Agogué et al., 2008; Tolar et al., 2013), or substrate and product of nitri cation, respectively, were wastewater treatment plants (e.g., Limpiyakorn et al., 2011; followed throughout the year 2015. At all water depths, the Mußmann et al., 2011; Sauder et al., 2012; Pan et al., concentrations of nitrate were at least one order of magni- – μ 2018). As a general trend, AOA typically outnumber AOB in tude higher (28 57 M) than of total ammonium – μ soils and marine waters, while AOB prevail in wastewater (0.01 0.84 M; Fig. 1). The water column was completely treatment plants, albeit exceptions to this trend exist oxygenated throughout the year, irrespective of the tempera- (Mußmann et al., 2011). How comammox fit into this picture ture gradient build-up during spring, summer and autumn is currently less clear because of their recent discovery. (Fig. 1). During the active phase of phytoplankton biomass However, first studies indicated a prevailing abundance in production as indicated by chlorophyll a maxima in the epi- oligotrophic habitats like groundwater wells (Pjevac et al., limnion (spring to autumn), ammonium and nitrate showed 2017) and the presence in soils, freshwater sediments and opposing depth gradients (Fig. 1). While nitrate was increas- biofilms, marine coastal environments, as well as wastewa- ing in concentration over depth, ammonium was decreasing. ter treatment plants (Daims et al., 2015; van Kessel et al., The latter indicated an ammonium sink in hypolimnetic fi 2015; Gulay et al., 2016; Pjevac et al., 2017; Xia et al., waters through nitri cation. This was corroborated by a fi 2018; Yu et al., 2018; Zheng et al., 2019). Based on the gross nitri cation estimate towards the end of the yearly phy- toplankton succession using a 15N-pool dilution method. apparent half-saturation constants (Km-values) for total −1 −1 + Here, a nitrification rate of 3.2 μmol l day could be esti- ammonium (NH3 +NH4 ), cultured AOA seem to better mated for water sampled at 85 m depth on 6 October 2015 adapted to lower (Km-values: 133 nM–42 μM; Martens- 15 Habbena et al., 2009; Kits et al., 2017) and cultured AOB (Fig. S1), albeit based on a high variation of residual Nin individual water replicates after 3 days of incubation. rather to higher total ammonium concentrations (Km-values: 30 μM–10 mM; Suzuki et al., 1974; Stehr et al., 1995; This translated into a threefold turnover of the total ammo- μ Martens-Habbena et al., 2009; Kits et al., 2017), which may nium pool per day. Incubations with 52 M 2-phenyl- explain their abundance ratios in the habitats mentioned 4,4,5,5-tetramethylimidazoline-3-oxide-1-oxyl (carboxy-PTIO) (13 October 2015, 85 m depth) as a selective inhibitor concen- above. The only determined Km-value of comammox bacte- ria (0.65 μM, Nitrospira inopinata) places this guild
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