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Environ Microbiol. 2019 Oct;21(10):3831-3854. doi: 10.1111/1462-2920.14732. Epub 2019 Jul 25.

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical sponge Ianthella basta.

Author information

1
Centre for Microbiology and Environmental Systems Science, Division of Microbial Ecology, University of Vienna, Austria.
2
Australian Institute of Marine Science, Townsville, Queensland, Australia.
3
Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St Lucia, Queensland, Australia.
4
Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, 9220, Aalborg, Denmark.
5
Institute of Marine Biotechnology e.V, Greifswald, Germany.
6
Institute of Pharmacy, Pharmaceutical Biotechnology, University of Greifswald, Greifswald, Germany.
7
Centre for Microbiology and Environmental Systems Science, Division of Computational Systems Biology, University of Vienna, Austria.
8
Institute of Microbiology, Microbial Proteomics, University of Greifswald, Greifswald, Germany.
9
Centre for Microbiology and Environmental Systems Science, Division of Terrestrial Ecosystem Research, University of Vienna, Austria.

Abstract

Marine sponges represent one of the few eukaryotic groups that frequently harbour symbiotic members of the Thaumarchaeota, which are important chemoautotrophic ammonia-oxidizers in many environments. However, in most studies, direct demonstration of ammonia-oxidation by these archaea within sponges is lacking, and little is known about sponge-specific adaptations of ammonia-oxidizing archaea (AOA). Here, we characterized the thaumarchaeal symbiont of the marine sponge Ianthella basta using metaproteogenomics, fluorescence in situ hybridization, qPCR and isotope-based functional assays. 'Candidatus Nitrosospongia ianthellae' is only distantly related to cultured AOA. It is an abundant symbiont that is solely responsible for nitrite formation from ammonia in I. basta that surprisingly does not harbour nitrite-oxidizing microbes. Furthermore, this AOA is equipped with an expanded set of extracellular subtilisin-like proteases, a metalloprotease unique among archaea, as well as a putative branched-chain amino acid ABC transporter. This repertoire is strongly indicative of a mixotrophic lifestyle and is (with slight variations) also found in other sponge-associated, but not in free-living AOA. We predict that this feature as well as an expanded and unique set of secreted serpins (protease inhibitors), a unique array of eukaryotic-like proteins, and a DNA-phosporothioation system, represent important adaptations of AOA to life within these ancient filter-feeding animals.

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