Co-occurring nitrifying symbiont lineages are vertically inherited and widespread in marine sponges

Bettina Glasl; Heidi M Luter; Katarina Damjanovic; Katharina Kitzinger; Anna J Mueller; Leonie Mahler; Joan Pamela Engelberts; Laura Rix; Jay T Osvatic; Bela Hausmann; Joana Séneca; Holger Daims; Petra Pjevac; Michael Wagner

doi:10.1093/ismejo/wrae069

Co-occurring nitrifying symbiont lineages are vertically inherited and widespread in marine sponges

ISME J. 2024 Apr 27:wrae069. doi: 10.1093/ismejo/wrae069. Online ahead of print.

Authors

Bettina Glasl¹, Heidi M Luter², Katarina Damjanovic², Katharina Kitzinger¹, Anna J Mueller^{1

3}, Leonie Mahler¹, Joan Pamela Engelberts^{4

5}, Laura Rix⁴, Jay T Osvatic^{6

7}, Bela Hausmann^{6

7}, Joana Séneca^{1

6}, Holger Daims¹, Petra Pjevac^{1

6}, Michael Wagner^{1

6

8}

Affiliations

¹ Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria.
² Australian Institute of Marine Science, Townsville, Australia.
³ Doctoral School in Microbiology and Environmental Science, University of Vienna, Vienna, Austria.
⁴ The University of Queensland, School of Chemistry and Molecular Biosciences, Australian Centre for Ecogenomics, Brisbane, Australia.
⁵ Centre for Microbiome Research, School of Biomedical Sciences, Queensland University of Technology, Translational Research Institute, Woolloongabba, Australia.
⁶ Joint Microbiome Facility of the Medical University of Vienna and the University of Vienna, Vienna, Austria.
⁷ Division of Clinical Microbiology, Department of Laboratory Medicine, Medical University of Vienna, Vienna, Austria.
⁸ Department of Chemistry and Bioscience, Aalborg University, Aalborg, Denmark.

PMID: 38676557
DOI: 10.1093/ismejo/wrae069

Abstract

Ammonia-oxidising archaea and nitrite-oxidising bacteria are common members of marine sponge microbiomes. They derive energy for carbon fixation and growth from nitrification - the aerobic oxidation of ammonia to nitrite and further to nitrate - and are proposed to play essential roles in the carbon and nitrogen cycling of sponge holobionts. In this study, we characterise two novel nitrifying symbiont lineages, Candidatus Nitrosokoinonia and Candidatus Nitrosymbion in the marine sponge Coscinoderma matthewsi using a combination of molecular tools, in situ visualisation, and physiological rate measurements. Both represent a new genus in the ammonia-oxidising archaeal class Nitrososphaeria and the nitrite-oxidising bacterial order Nitrospirales, respectively. Furthermore, we show that larvae of this viviparous sponge are densely colonised by representatives of Ca. Nitrosokoinonia and Ca. Nitrosymbion indicating vertical transmission. In adults, the representatives of both symbiont genera are located extracellularly in the mesohyl. Comparative metagenome analyses and physiological data suggest that ammonia-oxidising archaeal symbionts of the genus Ca. Nitrosokoinonia strongly rely on endogenously produced nitrogenous compounds (i.e., ammonium, urea, nitriles/cyanides, and creatinine) rather than on exogenous ammonium sources taken up by the sponge. Additionally, the nitrite-oxidising bacterial symbionts of the genus Ca. Nitrosymbion may reciprocally support the ammonia-oxidisers with ammonia via the utilisation of sponge-derived urea and cyanate. Comparative analyses of published environmental 16S rRNA gene amplicon data revealed that Ca. Nitrosokoinonia and Ca. Nitrosymbion are widely distributed and predominantly associated with marine sponges and corals, suggesting a broad relevance of our findings.

Keywords: Candidatus Nitrosokoinonia gen. Nov; Candidatus Nitrosymbion gen. Nov; ammonia-oxidising archaea; nitrite-oxidising bacteria; sponge microbiome; symbiont transmission.