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.

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).

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.

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).

My group has a long-standing interest in the interaction of marine sponges with their microbial symbionts (Hentschel et al. 2002, Taylor 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.