Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxiause asterix (*) to get italics

Brian W Strehlow, Astrid Schuster, Warren R Francis, Lisa Eckford-Soper, Beate Kraft, Rob McAllen, Ronni Nielsen, Susanne Mandrup, Donald E CanfieldPlease use the format "First name initials family name" as in "Marie S. Curie, Niels H. D. Bohr, Albert Einstein, John R. R. Tolkien, Donna T. Strickland"

2023

<p>Deoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, <em>Eurypon </em>sp. 2 and <em>Hymeraphia stellifera</em>, survive seasonal anoxia for months at a time. To understand their tolerance mechanisms, we performed differential gene expression analyses on the sponges, their mitochondria and their microbial symbionts under in situ conditions of normoxia, hypoxia and anoxia. Each species possessed a unique microbiome, but the microbiomes of each species were dominated by a species-specific <em>Thaumarchaeon </em>and a <em>Gammaproteobacterium</em>. Holobiont gene expression was species- and oxygen-level dependent, though there were some shared interspecific responses to deoxygenation. In general, few changes occurred in the expression of sponge metabolic genes as a function of oxygenation level, indicating that they may remain metabolically active under anoxia. However, ATP synthesis genes were significantly upregulated under hypoxia when compared to normoxia, and genes for DNA replication were downregulated. Mitochondrial gene expression was effectively unchanged under both hypoxia and anoxia. Nevertheless, both anoxia and hypoxia caused upregulation of heat shock proteins (HSPs), indicating cellular level adaptations to deoxygenation stress. A meta-analysis demonstrated that sponge transcriptional responses to anoxia were distinct from those displayed by other invertebrates while dormant, and the hypothesis of sponge dormancy under anoxia was not supported. <em>Thaumarchaeota </em>symbionts also upregulated stress response genes in hypoxia, while maintaining expression of oxygen-dependent metabolic pathways under hypoxia and anoxia. <em>Gammaproteobacteria </em>symbionts showed relatively few noteworthy changes in gene expression in response to anoxia but decreased metabolic gene expression in hypoxia. There was no clear evidence of upregulated anaerobic respiration in the transcriptomes of the sponge holobionts under anoxia or hypoxia. The tolerance of some sponges to prolonged anoxia warrants further investigation and could give them an advantage in future oceans following climate change as well as in ancient oceans when oxygen concentrations were lower than at present.</p>

https://doi.org/10.5281/zenodo.7418964, https://www.ncbi.nlm.nih.gov/bioproject/PRJNA893197You should fill this box only if you chose 'All or part of the results presented in this preprint are based on data'. URL must start with http:// or https://

https://doi.org/10.5281/zenodo.7418964You should fill this box only if you chose 'Scripts were used to obtain or analyze the results'. URL must start with http:// or https://

Sponge, Porifera, Thaumarchaeota, anoxia, deoxygenation, host-microbe interactions, microbiome

NonePlease indicate the methods that may require specialised expertise during the peer review process (use a comma to separate various required expertises).

Biology, Ecology, Genetics/Genomics, Invertebrates, Marine, Symbiosis

Dr. Benoit Paix, benoit.paix@natualis.nl, Dr. Aida Verdes, aida.verdes@mncn.csic.e, Dr. Heidi Luter, h.luter@aims.gov.au, Dr. Steven Robbins, s.robbins1@uq.edu.au, Dr. Bettina Glasl, bettina.glasl@univie.ac.at, Dr. Cristina Díez-Vives, cristinadiezvives@gmail.com, Dr. William Orsai, w.orsi@lrz.uni-muenchen.de, Dr. Torsten Thomas, t.thomas@unsw.edu.au, Dr. Kristina Bayer, kbayer@geomar.de, Dr. Nicole de Voogd, nicole.devoogd@naturalis.nl, Zbinden Magali suggested: Pierre Chevaldonné, pierre.chevaldonne@imbe.fr, Zbinden Magali suggested: Thierry Perez, thierry.perez@imbe.fr, Pierre Chevaldonné [pierre.chevaldonne@imbe.fr] suggested: Sorry, I'm running out of time currently, but most of all, I don't feel expert enough in the required field. I can suggest that you ask cesar.ruiz@imbe.fr or thierry.perez@imbe.fr they are working in this field and would have the proper expertise., Pierre Chevaldonné [pierre.chevaldonne@imbe.fr] suggested: Désolé Loïc, une prochaine fois., Pierre Chevaldonné [pierre.chevaldonne@imbe.fr] suggested: Regards, Pierre Chevaldonné [pierre.chevaldonne@imbe.fr] suggested: Pierre Chevaldonné, Cesar Ruiz [cesar.ruiz@imbe.fr] suggested: Thanks for your invitation but I do not have the experience in Transcriptomics to evaluate the paper. , Cesar Ruiz [cesar.ruiz@imbe.fr] suggested: Sincerely, César Ruiz , Kathrin Busch [kbusch@geomar.de] suggested: Dear Dr. Loïc Michel,, Kathrin Busch [kbusch@geomar.de] suggested: thank you very much for considering me as reviewer for the manuscript by Strehlow et al., Kathrin Busch [kbusch@geomar.de] suggested: I am currently overcommitted with work, so unfortunately have to decline., Kathrin Busch [kbusch@geomar.de] suggested: As alternative reviewers you may consider:, Kathrin Busch [kbusch@geomar.de] suggested: - Dr. Vassia Koutsouveli (vkoutsouveli@geomar.de, GEOMAR Helmholtz Centre for Ocean Research): expert on transcriptomic analyses of sponges, currently working in a sponge microbiology group, Kathrin Busch [kbusch@geomar.de] suggested: -Dr. Ana Riesgo (anariesgogil@gmail.com, Museo Nacional de Ciencias Naturales de Madrid): expert on sponge transcriptomic analyses of sponges, with experience in sponge microbiology, Kathrin Busch [kbusch@geomar.de] suggested: Best regards,, Kathrin Busch [kbusch@geomar.de] suggested: Kathrin Busch, Ana Riesgo suggested: Nathan James Kenny nathanjameskenny@gmail.com , Ana Riesgo suggested: Vasiliki Koutsouveli vassiakouts88@gmail.com , Vassia Koutsouveli [vkoutsouveli@geomar.de] suggested: Lara Schmittmann, lschmittmann@geomar.de No need for them to be recommenders of PCI Zool. Please do not suggest reviewers for whom there might be a conflict of interest. Reviewers are not allowed to review preprints written by close colleagues (with whom they have published in the last four years, with whom they have received joint funding in the last four years, or with whom they are currently writing a manuscript, or submitting a grant proposal), or by family members, friends, or anyone for whom bias might affect the nature of the review - see the code of conduct

2023-05-12 16:22:47

Loïc N. Michel

Maria Lopez Acosta