Prof. Dr. Dr. h. c. Michael Wagner

Michael Wagner
Vice Director of the Centre for Microbiology and Environmental Systems Science
University of Vienna
Department of Microbiology and Ecosystem Science
Division of Microbial Ecology
Djerassiplatz 1
A-1030 Vienna
Austria
Phone: +43 1 4277 91200

CV and output information is provided at the bottom of this page

We love to study the hidden world of microbes and are particularly excited to investigate microbes directly in their natural environment. My team has two major research foci. We are interested in all aspects of nitrification with a particular focus on the biology of ammonia-oxidizing archaea and bacteria as well as on complete nitrifiers of the genus Nitrospira (Comammox). Furthermore, we continuously develop innovative single cell tools for investigating the identity and function of individual microbial cells within their natural habitats.

COMPLETE NITRIFIERS OF THE GENUS NITROSPIRA (COMAMMOX) 

Since the first description of nitrifying microbes more than 100 years ago by Sergei Winogradsky nitrification was always thought to be conducted by the joint activity of two groups of microorganisms - the ammonia- and the nitrite-oxidizers. We recently discovered together with the group of Holger Daims that complete nitrifiers exist that can oxidize as single microorganisms ammonia to nitrate. These so-called Comammox (complete ammonia oxidizers) microorganisms are members of the genus Nitrospira and are widespread in terrestrial and freshwater habitats (Daims et al. 2015, Nature). In collaboration with Dr. Elena Lebedeva we obtained a pure culture from our Comammox enrichment and named it Nitrospira inopinata. Kinetic characterization of this comammox strain demonstrated that it has a higher affinity for ammonia than all studied ammonia-oxidizing bacteria (AOB) and most ammonia-oxidizing archaea (AOA). In contrast, its affinity for nitrite is rather low. Excitingly, N. inopinata has the highest biomass yield per mol of substrate oxidized among all nitrifiers analyzed. These results demonstrate that N. inopinata is very well adapted to oligotrophic conditions and that the comammox metabolism is highly efficient (Kits et al. 2017, Nature). In comparison to AOB, N. inopinata forms only very little N2O at low oxygen conditions and can thus be considered a "green nitrifier" (Kits et al. 2019; Nature Communications). Future research on the fascinating comammox organisms in our team will focus on revealing which environmental parameters select for comammox microbes in agricultural soil and wastewater treatment plants in order to pave the way for targeted manipulation of such nitriying communities. Furthermore, we plan to perform detailed strutural and functional characterization of the very unsusual complexes I and IV in the respiratory chain of comammox microbes in order to better understand the unusual physiology of these microbes. 

Now working on this theme: Chris Sedlaceck, Márton Palatinszky, Man-Young Jung (previously Mario PogodaJulia VierheiligDimitri KitsPing Han)

Collaboration partners: Elena Lebedeva (Russian Academy of Sciences), Mads AlbertsenPer Nielsen (Aalborg University, Denmark), Nico JehmlichMartin van Bergen (UFZ, Leipzig, Germany), Bernd Bendinger (TU Hamburg, Germany), Lisa Stein (University of Alberta, Canada)

Selected publications on this theme:

Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M. 2015. Complete nitrification by Nitrospira bacteria. Nature, 528: 504-509.

Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein LY, Daims H, Wagner M. 2017. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle Nature, 549: 269-272.

Kits KD, Jung MY, Vierheilig J, Pjevac P, Sedlacek CJ, Liu S, Herbold C, Stein LY, Richter A, Wissel H, Brüggemann N, Wagner M, Daims H. 2019. Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata. Nat Commun, 1: 1836.

Ammonia-oxidizing archaea and bacteria

Ammonia oxidation is a key step in the biogeochemical nitrogen cycle and is producing nitrite for nitrite-oxidizing or nitrite-reducing microbes. This process is of major importance for nitrogen cycling in the environment and a central step in efficient wastewater treatment, but also strongly contributes to fertilizer loss and N2O formation in agriculture. Microbial ammonia oxidation has been intensively investigated for decades, but until recently only two bacterial groups within the Proteobacteria were known to aerobically thrive on ammonia as substrate for growth. During the last decade it became apparent that members of the archaeal phylum Thaumarchaeota are also capable of ammonia-oxidation for energy generation. My lab investigates the evolution, physiology, and ecology of ammonia-oxidizing microbes. Our efforts in this field, that were also strongly supported by the ERC Advanced Grant project Nitricare, range from pure culture physiological studies to advanced single cell genomics approaches.

Recent projects:

  • We have obtained an enrichment of the ammonia-oxidizing thaumarchaeote Nitrososphaera gargensis and have analyzed this moderately thermophilic strain genomically (Spang et al., 2012). Interestingly, it produces F420 as a cofactor and has a more flexible central carbon metabolism than expected. In the meantime we succeeded in obtaining a pure culture of this strain. We are currently analysing the structure and function of its F420.

Now working on this theme: Chris Sedlaceck. Previously working on this theme: Roland Hatzenpichler, Alexander Galushko, Márton Palatinszky. Collaboration partner: Elena Lebedeva (Russian Academy of Sciences), Chris Greening (Monash University, Australia)

  • We recently demonstrated that N. gargensis is the first known organisms that can grow on cyanate as sole source of energy and reductant. While many other ammonia-oxidizers lack this capability, all genome-sequenced nitrite-oxidizers possess a cyanase for conversion of cyanate to ammonium and CO2. Using co-culture experiments we showed that cyanase-positive nitrite-oxidizers can team up with cyanase-negative ammonia oxidizers to enable growth of both partners on cyanate. This new type of interaction between nitrifiers via reciprocal feeding also showed that the first step in nitrification can in some cases be performed by nitrite-oxidizers (Palatinszky et al. 2015, Nature). Furthermore, we demonstrated that reciprocal feeding of nitrifiers also occurs with urea as substrate (Koch et al. 2015, PNAS). Interestingly, we could recently demonstrate cyanate conversion as a source of energy and nitrogen for marine thaumarchaeotes in the Gulf of Mexico that do not encode a canonical cyanase (Kitzinger et al. 2019).

    Now working on this theme: Katharina Kitzinger (previously Alexander Galushko, Márton PalatinszkyPing HanMario PogodaMaria Mooshammer)
    Collaboration partners: Marcel Kuypers (MPI Bremen, Germany), Nico Jehmlich, Martin van Bergen (UFZ, Leipzig, Germany)
     

  • In collaboration with Yujie Men and Kathrin Fenner from the EAWAG in Switzerland we investigate micropollutant degradation by ammonia-oxidizing bacteria and archaea.
    Previously working on this theme: Ping Han
     
  • We have shown that close relatives of N. gargensis in an industrial wastewater treatment plant encode and express amoA, but obtain their energy from substrates other than ammonia (Mussman et al. 2011, PNAS). Using single-cell, cultivation and meta-omic techniques we are characterizing thauamarchaeotes in various municipal and industrial wastewater treatment plants to better understand (i) their contribution to nitrification in these systems and (ii) their physiological versatility.

    Now working on this theme: Julia Vierheilig.
    Collaboration partners: Josh Neufeld and Laura Sauder (University of Waterloo, Canada), and Ian Head (Newcastle, Uk)
     

  • We investigate the diversity of ammonia-oxidizing microbes in wastewater treatment plants by single microcolony isotope labeling, subsequent Raman sorting and single microcolony genomics. As closely attached interaction partners of the ammonia-oxidizers are also sorted, this approach does not only reveal genomic information of the active members of this guild, but also enables genomic characterization of nitrifier interaction partners in the wilderness. This project is supported by an ETOP- and a CSP-project of the JGI and is performed in collaboration with Tanja Woyke.
    In order to establish an encompassing framework for comparative genomics of sorted ammonia oxidizers, we are currently sequencing the genomes of many cultures strains of this guild. This project is performed in collaboration with Andreas Pommerening-Röser (University of Hamburg, Germany) and Tanja Woyke from the JGI (Walnut Creek, USA).

    Now working on this theme: Márton Palatinszky, Craig Herbold (previously Tae Kwon Lee, Esther Mader, Adrian Berger, Julius Simonis, )
     

  • My group has a long-standing interest in the interaction of marine sponges with their microbial symbionts (Hentschel et al. 2002Taylor et al. 2007, Webster et al. 2010). Using Ianthella basta from the Great Barrier Reef in Australia as model sponge we investigate by metagenomics, metaproteomics, and isotope labeling techniques the physiological interaction between this sponge and its symbionts. In contrast to many other sponges, I. basta harbors only three abundant symbionts and one of them is an ammonia-oxidizing member of the Thaumarchaeotes. This project has been supported by the Marie Curie International Training Networks Symbiomics.

    Now working on this theme: Florian Moeller
    Collaboration partners: Nicole Webster (AIMS, Australia), Thomas Schweder, Stephanie Markert (University of Greifswald, Germany), Mads Albertsen, Per Nielsen (Aalborg University, Denmark), Thomas Rattei, and Andreas Richter (University of Vienna, Austria)

 

Selected publications on this theme:

Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA 105: 2134-2139.

Kitzinger K, Padilla CC, Marchant HK, Hach PF, Herbold CW, Kidane AT, Könneke M, Littmann S, Mooshammer M, Niggemann J, Petrov S, Richter A, Stewart FJ, Wagner M, Kuypers MMM, Bristow LA. 2019. Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. Nat Microbiol, 2: 234-243

Koch H, Lücker S, Albertsen M, Kitzinger K, Herbold C, Spieck E, Nielsen PH, Wagner M, Daims H. 2015. Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc Natl Acad Sci U S A, 112: 11371-11376.

Mußmann M, Brito I, Pitcher A, Damsté JSS, Hatzenpichler R, Richter A, Nielsen JL, Nielsen PH, Müller A, Daims H, Wagner M, Head IM. 2011. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc. Natl. Acad. Sci. USA 108: 16771-16776.

Palatinszky M, Herbold C, Jehmlich N, Pogoda M, Han P, von Bergen M, Lagkouvardos I, Karst SM, Galushko A, Koch H, Berry D, Daims H, Wagner M. 2015. Cyanate as an energy source for nitrifiers. Nature 524:105-108.

Pester M, Schleper C, Wagner M. 2011. The Thaumarchaeota: An Emerging View of their Phylogeny and Ecophysiology. Curr. Opin. Microbiol. 14: 300-306.

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. Environ. Microbiol. 14: 525-539.

Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva EV, Rattei T, Böhm C, Schmid M, Galushko A, Hatzenpichler R, Weinmaier T, Daniel R, Schleper C, Spieck E, Streit W, Wagner M. 2012. The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: Insights into metabolic versatility and environmental adaptations. Environ. Microbiol. 14: 3122-45.

What are they doing there? New single cell tools for functional analyses of microbes in their ecosystems

My team has a long-standing interest in the development of methods for functional analyses of microbes within complex microbial communities (Wagner et al. 1998; Adamczyk et al. 2003). For example, we pioneered the combination of FISH and microautoradiography (Lee et al., 1999) that enabled microbial ecologists for the first time to observe substrate utilization of uncultured individual microbial cells in their natural habitat. Currently, second generation methods for single cell isotope probing mainly using 13C-, 15N and 2H-labeled compounds are developed and combined with single cell genomics approaches. For the detection of isotopes within microbial cells we use nanometer-scale secondary ion mass spec­trometry (NanoSIMS) and Raman microspectroscopy.

NanoSIMS. NanoSIMS imaging is perfectly suited to measure and visualize the distribution of virtually any elements and their stable isotopes of interest in microbial cells. We run in our team since 2010 a CAMECA NanoSIMS 50L (the only NanoSIMS instrument in Austria) that offers a spatial resolution for element/ isotope mapping down to 50 nm and thus even allows highly sen­sitive analyses at the sub-cellular level. The NanoSIMS 50L is equipped with Cs+ and O- primary ion sources, an electron gun for analysis of insulating samples, a secondary electron detector, and a magnetic sector mass analyser with a large version of the magnet and a multi-collection system of 7 detectors all equipped with Faraday cups and electron multiplier detectors. In microbial ecology we combine NanoSIMS with stable isotope prob­ing and cell identification techniques such as fluo­rescence in situ hybridization to obtain previously inaccessible information about the functional role of microorganisms in their environment. Using this approach, previously unrecognized physio­logical properties of bacteria and archaea thriving in soils, microbial mats, deep groundwater sam­ples and within corals as well as mice guts could be deciphered.

Now working on this theme: Arno Schintlmeister

Selected publications on this theme:

Berry D, Stecher B, Schintlmeister A, Reichert J, Brugiroux S, Wildd B, Wanek W, Richter A, Rauch I, Decker T, Loy A, Wagner M. 2013. Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc. Natl. Acad. Sci. USA 110: 4720-4725.

Koch H, Galushko A, Albertsen M, Schintlmeister A, Gruber-Dorninger C, Lücker S, Pelletier E, Le Paslier D, Spieck E, Richter A, Nielsen PH, Wagner M, Daims H. 2014. Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science 345: 1052-1054.

Woebken D, Burow L, Behnam F, Mayali X, Schintlmeister A, Fleming E, Prufert-Bebout L, Singer S, López Cortés A, Hoehler T, Pett-Ridge J, Spormann A, Wagner M, Weber P, Bebout B. 2015. Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach. ISME J. 9: 485-496.

 

Raman microspectroscopy. In my lab we develop new confocal Raman microspectrocopy-based methods for functional analyses of microbes in complex ecosystems. Raman microspectroscopy has single cell resolution and is nondestructive. It enables us to record within seconds a chemical fingerprint of a microbial cell that reveals the presence of defined storage compounds (Milucka et al., 2012), cytochromes and pigments. Raman microspectroscopy can be directly combined with FISH (Huang et al. 2007) for simultaneous identification of the analyzed microbes.  Furthermore, Raman microspectroscopy can be applied to detect and quantify the incorporation of stable isotopes in individual microbial cells and is the most straightforward technique to perform single cell stable isotope probing experiments with complex microbial communities. In addition to detection of 13C-labeled cells (Huang et al. 2007), we recently applied Raman microspectroscopy for tracking the incorporation of deuterium from heavy water in microbial cells in order to measure their activity (Berry et al. 2015). Excitingly, Raman spectra of microbial cells can also be recorded while holding them with an optical tweezer. Subsequently, cells can then be sorted according to their Raman spectrum for single cell genomics or cultivation (Berry et al. 2015). In collaboration with Roman Stocker (ETH, Switzerland) we have developed a microfluidics chamber for high-throughput sorting of microbial cells according to their Raman spectra for directly combining single cell stable isotope probing and single cell genomics or cultivation (Lee et al. 2019).

At DOME two cutting edge confocal Raman microspectrometer are available. A LabRAM HR800 and an HR Evolution (both from Horiba Jobin-Yvon). Availabe lasers are a 532-nm neodymium-yttrium aluminium garnet laser,  a pulsed 532-nm laser, a 785 nm laser, and a 1,064-nm laser for optical trapping.

Now working on this theme: Márton Palatinszky, Markus Schmid, (previously Tae Kwon Lee, Christoph Böhm, Esther Mader)

 

Selected publications on this theme:

Berry D, Mader E, Lee TK, Woebken D, Wang Y, Zhu D, Palatinszky M, Schintlmeister A, Schmid MC, Hanson BT, Shterzer , Mizrahi I, Rauch I, Decker T, Bocklitz T, Popp J, Gibson CM, Fowler PW, Huang WE, Wagner M. 2015. Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. Proc. Natl. Acad. Sci. USA  Jan 13;112(2):E194-203.

Huang WE, Stoecker K, Griffiths R, Newbold L, Daims H, Whiteley AS, Wagner M. 2007. Raman-FISH: Combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ. Microbiol. 9: 1878-1889.

Milucka J, Ferdelman TG, Polerecky L, Franzke D, Wegener G, Schmid M, Lieberwirth I, Wagner M, Widdel F, Kuypers MMM. 2012. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491: 541-546.

Lee KS, Palatinszky M, Pereira FC, Nguyen J, Fernandez VI, Mueller AJ, Menolascina F, Daims H, Berry D, Wagner M, Stocker R. 2019. An automated Raman-based platform for the sorting of live cells by functional properties. Nat Microbiol 6: 1035-1048.

THE GROUP

Joining the team

Information on open research positions can be found here. If you are interested in joining our team with your own fellowship, please check out our PhD & postdoc program and get in touch with Michael for details.