Background: Methanotrophy by the sponge-hosted microbiome has been mainly reported in the ecological context of deep-sea hydrocarbon seep niches where methane is either produced geothermically or via anaerobic methanogenic archaea inhabiting the sulfate-depleted sediments. However, methane-oxidizing bacteria from the candidate phylum Binatota have recently been described and shown to be present in oxic shallow-water marine sponges, where sources of methane remain undescribed. Results: Here, using an integrative -omics approach, we provide evidence for sponge-hosted bacterial methane synthesis occurring in fully oxygenated shallow-water habitats. Specifically, we suggest methane generation occurs via at least two independent pathways involving methylamine and methylphosphonate transformations that, concomitantly to aerobic methane production, generate bioavailable nitrogen and phosphate, respectively. Methylphosphonate may be sourced from seawater continuously filtered by the sponge host. Methylamines may also be externally sourced or, alternatively, generated by a multi-step metabolic process where carnitine, derived from sponge cell debris, is transformed to methylamine by different sponge-hosted microbial lineages. Finally, methanotrophs specialized in pigment production, affiliated to the phylum Binatota, may provide a photoprotective function, closing a previously undescribed C1-metabolic loop that involves both the sponge host and specific members of the associated microbial community. Conclusion: Given the global distribution of this ancient animal lineage and their remarkable water filtration activity, sponge-hosted methane cycling may affect methane supersaturation in oxic coastal environments. Depending on the net balance between methane production and consumption, sponges may serve as marine sources or sinks of this potent greenhouse gas. [MediaObject not available: see fulltext.]
|State||Published - 10 Mar 2023|
Bibliographical noteFunding Information:
Livio Steindler is warmly thanked for assisting us as captain and for providing his sailing boat Colpo de Fulmine II for the sponge sampling. We thank the “Area51 Diving School Trieste” for supporting all the dive equipment in this research and assisting with the scientific dives. Cláudia Ferreira is acknowledged for the design of Fig. 6. Dr. Stefan Green and Dr. Kevin J. Kunstman from the Sequencing Core at the University of Illinois at Chicago (UIC) are acknowledged for advice on library preparation protocols and for sequencing. We thank Kelly Paglia and Christopher Brydges at the UC Davis metabolomic center for technical support with our sponge tissue analyses.
This study was funded by the Gordon and Betty Moore Foundation, through Grant GBMF9352, and by the Israel Science Foundation [grant no. 1243/16] titled “Identification of molecular mechanisms underlying sponge-microbiome symbiosis.” GAR was supported by a Zuckerman Postdoctoral research fellowship.
© 2023, The Author(s).
- Aerobic methane synthesis
- Aplysina aerophoba
- Candidate phylum Binatota
- Petrosia ficiformis
ASJC Scopus subject areas
- Microbiology (medical)