Section: Zoology
Topic: Ecology, Genetics/genomics, Microbiology

Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia

10.24072/pcjournal.410 - Peer Community Journal, Volume 4 (2024), article no. e43.

Get full text PDF Peer reviewed and recommended by PCI
article image

Deoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, Eurypon sp. 2 and Hymeraphia stellifera, 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 Thaumarchaeon and a Gammaproteobacterium. 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. Thaumarchaeota symbionts also upregulated stress response genes in hypoxia, while maintaining expression of oxygen-dependent metabolic pathways under hypoxia and anoxia. Gammaproteobacteria 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.

Published online:
DOI: 10.24072/pcjournal.410
Type: Research article
Keywords: Sponges, deoxygenation, microbiome, gene expression, marine, Thaumarchaeota, Gammaproteobacteria 

Strehlow, Brian W. 1, 2; Schuster, Astrid 1; Francis, Warren R. 1; Eckford-Soper, Lisa 1; Kraft, Beate 1; McAllen, Rob 3; Nielsen, Ronni 4; Mandrup, Susanne 4; Canfield, Donald E. 1

1 Nordcee, Department of Biology, University of Southern Denmark, Odense M, Denmark
2 Littoral Environnement et Sociétés (LIENSs), UMR 7266 CNRS - La Rochelle Université, 2 Rue Olympe de Gouges, 17000, La Rochelle, France
3 School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland
4 Functional Genomics and Metabolism Research Unit, Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Strehlow, Brian W. and Schuster, Astrid and Francis, Warren R. and Eckford-Soper, Lisa and Kraft, Beate and McAllen, Rob and Nielsen, Ronni and Mandrup, Susanne and Canfield, Donald E.},
     title = {Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia},
     journal = {Peer Community Journal},
     eid = {e43},
     publisher = {Peer Community In},
     volume = {4},
     year = {2024},
     doi = {10.24072/pcjournal.410},
     language = {en},
     url = {}
AU  - Strehlow, Brian W.
AU  - Schuster, Astrid
AU  - Francis, Warren R.
AU  - Eckford-Soper, Lisa
AU  - Kraft, Beate
AU  - McAllen, Rob
AU  - Nielsen, Ronni
AU  - Mandrup, Susanne
AU  - Canfield, Donald E.
TI  - Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
JO  - Peer Community Journal
PY  - 2024
VL  - 4
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.410
LA  - en
ID  - 10_24072_pcjournal_410
ER  - 
%0 Journal Article
%A Strehlow, Brian W.
%A Schuster, Astrid
%A Francis, Warren R.
%A Eckford-Soper, Lisa
%A Kraft, Beate
%A McAllen, Rob
%A Nielsen, Ronni
%A Mandrup, Susanne
%A Canfield, Donald E.
%T Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia
%J Peer Community Journal
%D 2024
%V 4
%I Peer Community In
%R 10.24072/pcjournal.410
%G en
%F 10_24072_pcjournal_410
Strehlow, Brian W.; Schuster, Astrid; Francis, Warren R.; Eckford-Soper, Lisa; Kraft, Beate; McAllen, Rob; Nielsen, Ronni; Mandrup, Susanne; Canfield, Donald E. Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia. Peer Community Journal, Volume 4 (2024), article  no. e43. doi : 10.24072/pcjournal.410.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.zool.100211

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Akiva, E.; Copp, J. N.; Tokuriki, N.; Babbitt, P. C. Evolutionary and molecular foundations of multiple contemporary functions of the nitroreductase superfamily, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 45 | DOI

[2] Altieri, A. H.; Harrison, S. B.; Seemann, J.; Collin, R.; Diaz, R. J.; Knowlton, N. Tropical dead zones and mass mortalities on coral reefs, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 14, pp. 3660-3665 | DOI

[3] Bayer, K.; Busch, K.; Kenchington, E.; Beazley, L.; Franzenburg, S.; Michels, J.; Hentschel, U.; Slaby, B. M. Microbial Strategies for Survival in the Glass Sponge Vazella pourtalesii, mSystems, Volume 5 (2020) no. 4 | DOI

[4] Bell, J. J.; Bennett, H. M.; Rovellini, A.; Webster, N. S. Sponges to Be Winners under Near-Future Climate Scenarios, BioScience, Volume 68 (2018) no. 12, pp. 955-968 | DOI

[5] Bell, J. J.; Barnes, D. K. A. The distribution and prevalence of sponges in relation to environmental gradients within a temperate sea lough: inclined cliff surfaces, Diversity and Distributions, Volume 6 (2000) no. 6, pp. 305-323 | DOI

[6] Bennett, H. M.; Altenrath, C.; Woods, L.; Davy, S. K.; Webster, N. S.; Bell, J. J. Interactive effects of temperature and <scp>pCO</scp>2 on sponges: from the cradle to the grave, Global Change Biology, Volume 23 (2016) no. 5, pp. 2031-2046 | DOI

[7] Bergquist, P. R. The marine fauna of new zealand: porifera, demospongiae, part 1 (tetractinomorpha and lithistida), New Zealand Oceanographic Institute Memoir, Volume 37 (1968), pp. 27-28 (

[8] Bosc, L. Histoire naturelle des crustacés contenant leur description et leurs moeurs; avec figures dessinées, d'après nature, Chez Deterville, 1802, pp. 1-296 | DOI

[9] Bowerbank, J. S. On the anatomy and physiology of the spongiadae. part i. on the spicula, Transactions of the Royal Society, Volume 148 (1858), pp. 279-332 (

[10] Bowerbank, J. S. A monograph of the British spongiadae, 1, Ray Society, London, 1864, 1-290 pages (

[11] Breitburg, D.; Levin, L. A.; Oschlies, A.; Grégoire, M.; Chavez, F. P.; Conley, D. J.; Garçon, V.; Gilbert, D.; Gutiérrez, D.; Isensee, K.; Jacinto, G. S.; Limburg, K. E.; Montes, I.; Naqvi, S. W. A.; Pitcher, G. C.; Rabalais, N. N.; Roman, M. R.; Rose, K. A.; Seibel, B. A.; Telszewski, M.; Yasuhara, M.; Zhang, J. Declining oxygen in the global ocean and coastal waters, Science, Volume 359 (2018) no. 6371 | DOI

[12] Chance, B. Reaction of Oxygen with the Respiratory Chain in Cells and Tissues, The Journal of General Physiology, Volume 49 (1965) no. 1, pp. 163-188 | DOI

[13] Chandel, N. S.; Schumacker, P. T. Cellular oxygen sensing by mitochondria: old questions, new insight, Journal of Applied Physiology, Volume 88 (2000) no. 5, pp. 1880-1889 | DOI

[14] Dendy, A. Report on the sponges collected by Professor Herdman, at Ceylon, in 1902 In: Report to the Government of Ceylon on the Pearl Oyster Fisheries of the Gulf of Manaar, Volume 3, Royal Society (1905), pp. 57-246 (

[15] Diaz, R. J.; Rosenberg, R. Spreading Dead Zones and Consequences for Marine Ecosystems, Science, Volume 321 (2008) no. 5891, pp. 926-929 | DOI

[16] Dixon, G. B.; Davies, S. W.; Aglyamova, G. V.; Meyer, E.; Bay, L. K.; Matz, M. V. Genomic determinants of coral heat tolerance across latitudes, Science, Volume 348 (2015) no. 6242, pp. 1460-1462 | DOI

[17] Dohrmann, M.; Wörheide, G. Dating early animal evolution using phylogenomic data, Scientific Reports, Volume 7 (2017) no. 1 | DOI

[18] D’Souza, A. R.; Minczuk, M. Mitochondrial transcription and translation: overview, Essays in Biochemistry, Volume 62 (2018) no. 3, pp. 309-320 | DOI

[19] Edler, D.; Klein, J.; Antonelli, A.; Silvestro, D. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML, Methods in Ecology and Evolution, Volume 12 (2020) no. 2, pp. 373-377 | DOI

[20] Efremova, S. M.; Margulis, B. A.; Guzhova, I. V.; Itskovich, V. B.; Lauenroth, S.; Müller, W. E.; Schröder, H. C. Heat shock protein Hsp70 expression and DNA damage in Baikalian sponges exposed to model pollutants and wastewater from Baikalsk Pulp and Paper Plant, Aquatic Toxicology, Volume 57 (2002) no. 4, pp. 267-280 | DOI

[21] Ellington, W. R. Metabolic Responses of the Sea Anemone Bunodosoma cavernata (Bosc) to Declining Oxygen Tensions and Anoxia, Physiological Zoology, Volume 55 (1982) no. 3, pp. 240-249 | DOI

[22] Feuda, R.; Dohrmann, M.; Pett, W.; Philippe, H.; Rota-Stabelli, O.; Lartillot, N.; Wörheide, G.; Pisani, D. Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals, Current Biology, Volume 27 (2017) no. 24 | DOI

[23] Francis, W. Make interactive plot of contigs in genomes or metagenomes, Gihub, 2020 (

[24] Francis, W. General sequence processing scripts, bitbucket, 2020 (

[25] Gong, Z.-J.; Wu, Y.-Q.; Miao, J.; Duan, Y.; Jiang, Y.-L.; Li, T. Global Transcriptome Analysis of Orange Wheat Blossom Midge, Sitodiplosis mosellana (Gehin) (Diptera: Cecidomyiidae) to Identify Candidate Transcripts Regulating Diapause, PLoS ONE, Volume 8 (2013) no. 8 | DOI

[26] Görlach, A.; Dimova, E. Y.; Petry, A.; Martínez-Ruiz, A.; Hernansanz-Agustín, P.; Rolo, A. P.; Palmeira, C. M.; Kietzmann, T. Reactive oxygen species, nutrition, hypoxia and diseases: Problems solved?, Redox Biology, Volume 6 (2015), pp. 372-385 | DOI

[27] Grabherr, M. G.; Haas, B. J.; Yassour, M.; Levin, J. Z.; Thompson, D. A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; Chen, Z.; Mauceli, E.; Hacohen, N.; Gnirke, A.; Rhind, N.; di Palma, F.; Birren, B. W.; Nusbaum, C.; Lindblad-Toh, K.; Friedman, N.; Regev, A. Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nature Biotechnology, Volume 29 (2011) no. 7, pp. 644-652 | DOI

[28] Grant, R. Notice of a new zoophyte (Cliona celata Gr.) from the Firth of Forth, New Philosophical Journal (1826), pp. 78-81 (

[29] Grant, R. Animal Kingdom, The Cyclopaedia of Anatomy and Physiology, Sherwood, Gilbert, and Piper, 1836, pp. 107-118

[30] Grasshoff, K.; Kremling, K.; Ehrhardt, M. Methods of Seawater Analysis, Wiley, New York, 1999, 600 pages | DOI

[31] Gunda, V. G.; Janapala, V. R. Effects of dissolved oxygen levels on survival and growth in vitro of Haliclona pigmentifera (Demospongiae), Cell and Tissue Research, Volume 337 (2009) no. 3, pp. 527-535 | DOI

[32] Guzman, C.; Conaco, C. Gene Expression Dynamics Accompanying the Sponge Thermal Stress Response, PLOS ONE, Volume 11 (2016) no. 10 | DOI

[33] Hochachka, P.; Lutz, P. Mechanism, origin, and evolution of anoxia tolerance in animals☆, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Volume 130 (2001) no. 4, pp. 435-459 | DOI

[34] Hoffmann, F.; Larsen, O.; Thiel, V.; Rapp, H. T.; Pape, T.; Michaelis, W.; Reitner, J. An Anaerobic World in Sponges, Geomicrobiology Journal, Volume 22 (2005) no. 1-2, pp. 1-10 | DOI

[35] Hoffmann, F.; Radax, R.; Woebken, D.; Holtappels, M.; Lavik, G.; Rapp, H. T.; Schläppy, M.; Schleper, C.; Kuypers, M. M. M. Complex nitrogen cycling in the sponge Geodia barretti, Environmental Microbiology, Volume 11 (2009) no. 9, pp. 2228-2243 | DOI

[36] Huerta-Cepas, J.; Szklarczyk, D.; Forslund, K.; Cook, H.; Heller, D.; Walter, M. C.; Rattei, T.; Mende, D. R.; Sunagawa, S.; Kuhn, M.; Jensen, L. J.; von Mering, C.; Bork, P. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences, Nucleic Acids Research, Volume 44 (2015) no. D1 | DOI

[37] Hughes, D. J.; Alderdice, R.; Cooney, C.; Kühl, M.; Pernice, M.; Voolstra, C. R.; Suggett, D. J. Coral reef survival under accelerating ocean deoxygenation, Nature Climate Change, Volume 10 (2020) no. 4, pp. 296-307 | DOI

[38] Huntley, M. A.; Larson, J. L.; Chaivorapol, C.; Becker, G.; Lawrence, M.; Hackney, J. A.; Kaminker, J. S. ReportingTools: an automated result processing and presentation toolkit for high-throughput genomic analyses, Bioinformatics, Volume 29 (2013) no. 24, pp. 3220-3221 | DOI

[39] Johnston, G. A history of British sponges and lithophytes, W.H. Lizars, 1842, pp. 146-147

[40] Jormakka, M.; Byrne, B.; Iwata, S. Formate dehydrogenase – a versatile enzyme in changing environments, Current Opinion in Structural Biology, Volume 13 (2003) no. 4, pp. 418-423 | DOI

[41] Katoh, K. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Research, Volume 30 (2002) no. 14, pp. 3059-3066 | DOI

[42] Keeling, R. F.; Körtzinger, A.; Gruber, N. Ocean Deoxygenation in a Warming World, Annual Review of Marine Science, Volume 2 (2010) no. 1, pp. 199-229 | DOI

[43] Kelly‐Borges, M.; Bergquist, P. R. Revision of Southwest Pacific Polymastiidae (Porifera: Demospongiae: Hadromerida) with descriptions of new species of Polymastia Bowerbank,Tylexocladus Topsent, and Acanthopolymastia gen. nov. from New Zealand and the Norfolk Ridge, New Caledonia, New Zealand Journal of Marine and Freshwater Research, Volume 31 (1997) no. 3, pp. 367-402 | DOI

[44] Kirchman, D. L. Dead Zones, Oxford University Press, 2021 | DOI

[45] Kolde, R. Pheatmap: Pretty Heatmaps. R-package, 2013 (

[46] Kraft, B.; Jehmlich, N.; Larsen, M.; Bristow, L.; Könneke, M.; Thamdrup, B. C. D. Oxygen and nitrogen production by an ammonia-oxidizing archaeon, Science, Volume 375, pp. 97-100 | DOI

[47] Kraft, B.; Jehmlich, N.; Larsen, M.; Bristow, L.; Könneke, M.; Thamdrup, B.; Canfield, D. E. Oxygen production by an ammonia-oxidizing archaeon, bioRxiv | DOI

[48] Kumala, L.; Larsen, M.; Glud, R. N.; Canfield, D. E. Spatial and temporal anoxia in single-osculum Halichondria panicea demosponge explants studied with planar optodes, Marine Biology, Volume 168 (2021) no. 12 | DOI

[49] Langmead, B.; Salzberg, S. L. Fast gapped-read alignment with Bowtie 2, Nature Methods, Volume 9 (2012) no. 4, pp. 357-359 | DOI

[50] Larade, K.; Storey, K. Living without Oxygen: Anoxia-Responsive Gene Expression and Regulation, Current Genomics, Volume 10 (2009) no. 2, pp. 76-85 | DOI

[51] Lemmens, L.; Maklad, H. R.; Bervoets, I.; Peeters, E. Transcription Regulators in Archaea: Homologies and Differences with Bacterial Regulators, Journal of Molecular Biology, Volume 431 (2019) no. 20, pp. 4132-4146 | DOI

[52] Lévi, C. Sur une nouvelle classification des Démosponges, Compte rendu hebdomadaire des séances de l'Académie des sciences, Volume 236 (1953), pp. 853-855 (

[53] Levin, L. A. Manifestation, Drivers, and Emergence of Open Ocean Deoxygenation, Annual Review of Marine Science, Volume 10 (2018) no. 1, pp. 229-260 | DOI

[54] Leys, S. P.; Kahn, A. S. Oxygen and the Energetic Requirements of the First Multicellular Animals, Integrative and Comparative Biology, Volume 58 (2018) no. 4, pp. 666-676 | DOI

[55] Li, D.; Luo, R.; Liu, C.-M.; Leung, C.-M.; Ting, H.-F.; Sadakane, K.; Yamashita, H.; Lam, T.-W. MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices, Methods, Volume 102 (2016), pp. 3-11 | DOI

[56] Li, Z.; Srivastava, P. Heat‐Shock Proteins, Current Protocols in Immunology, Volume 58 (2003) no. 1 | DOI

[57] Longmuir, I. S. Respiration rate of rat-liver cells at low oxygen concentrations, Biochemical Journal, Volume 65 (1957) no. 2, pp. 378-382 | DOI

[58] López-Legentil, S.; Song, B.; McMurray, S. E.; PAWLIK, J. R. Bleaching and stress in coral reef ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta, Molecular Ecology, Volume 17 (2008) no. 7, pp. 1840-1849 | DOI

[59] Löscher, C. R.; Kock, A.; Könneke, M.; LaRoche, J.; Bange, H. W.; Schmitz, R. A. Production of oceanic nitrous oxide by ammonia-oxidizing archaea, Biogeosciences, Volume 9 (2012) no. 7, pp. 2419-2429 | DOI

[60] Love, M. I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biology, Volume 15 (2014) no. 12 | DOI

[61] Lynch, M.; Marinov, G. K. The bioenergetic costs of a gene, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 51, pp. 15690-15695 | DOI

[62] MacRae, T. H. Gene expression, metabolic regulation and stress tolerance during diapause, Cellular and Molecular Life Sciences, Volume 67 (2010) no. 14, pp. 2405-2424 | DOI

[63] Magnet, S.; Dubost, L.; Marie, A.; Arthur, M.; Gutmann, L. Identification of the<scp>l,d</scp>-Transpeptidases for Peptidoglycan Cross-Linking inEscherichia coli, Journal of Bacteriology, Volume 190 (2008) no. 13, pp. 4782-4785 | DOI

[64] Matz, M. V. Assembly and annotation of transcriptomes de novo, Github, 2015 (

[65] Medini, H.; Cohen, T.; Mishmar, D. Mitochondrial gene expression in single cells shape pancreatic beta cells' sub-populations and explain variation in insulin pathway, Scientific Reports, Volume 11 (2021) no. 1 | DOI

[66] Meyer, E. A collection of scripts for analyzing transcriptome assemblies., Github (2016) (

[67] Micaroni, V.; McAllen, R.; Turner, J.; Strano, F.; Morrow, C.; Picton, B.; Harman, L.; Bell, J. J. Vulnerability of Temperate Mesophotic Ecosystems (TMEs) to environmental impacts: Rapid ecosystem changes at Lough Hyne Marine Nature Reserve, Ireland, Science of The Total Environment, Volume 789 (2021) | DOI

[68] Micaroni, V.; Strano, F.; McAllen, R.; Woods, L.; Turner, J.; Harman, L.; Bell, J. J. Adaptive strategies of sponges to deoxygenated oceans, Global Change Biology, Volume 28 (2021) no. 6, pp. 1972-1989 | DOI

[69] Michel, L. N. Future oceanic conditions could leave sponge holobionts breathless – but they won’t let that stop them, Peer Community in Zoology (2023) | DOI

[70] Mills, D. B.; Francis, W. R.; Vargas, S.; Larsen, M.; Elemans, C. P.; Canfield, D. E.; Wörheide, G. The last common ancestor of animals lacked the HIF pathway and respired in low-oxygen environments, eLife, Volume 7 (2018) | DOI

[71] Mills, D. B.; Ward, L. M.; Jones, C.; Sweeten, B.; Forth, M.; Treusch, A. H.; Canfield, D. E. Oxygen requirements of the earliest animals, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 11, pp. 4168-4172 | DOI

[72] Moeller, F. U.; Webster, N. S.; Herbold, C. W.; Behnam, F.; Domman, D.; Albertsen, M.; Mooshammer, M.; Markert, S.; Turaev, D.; Becher, D.; Rattei, T.; Schweder, T.; Richter, A.; Watzka, M.; Nielsen, P. H.; Wagner, M. Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical spongeIanthella basta, Environmental Microbiology, Volume 21 (2019) no. 10, pp. 3831-3854 | DOI

[73] Moitinho-Silva, L.; Díez-Vives, C.; Batani, G.; Esteves, A. I. S.; Jahn, M. T.; Thomas, T. Integrated metabolism in sponge–microbe symbiosis revealed by genome-centered metatranscriptomics, The ISME Journal, Volume 11 (2017) no. 7, pp. 1651-1666 | DOI

[74] Nielsen, C. Six major steps in animal evolution: are we derived sponge larvae?, Evolution &amp; Development, Volume 10 (2008) no. 2, pp. 241-257 | DOI

[75] Pallas, P. S. Elenchus zoophytorum sistens generum adumbrationes generaliores et specierum cognitarum succintas descriptiones, cum selectis auctorum synonymis, Fransiscum Varrentrapp, Hagae, 1766, 451 pages | DOI

[76] Pawlik, J. R.; Burkepile, D. E.; Thurber, R. V. A Vicious Circle? Altered Carbon and Nutrient Cycling May Explain the Low Resilience of Caribbean Coral Reefs, BioScience, Volume 66 (2016) no. 6, pp. 470-476 | DOI

[77] Plese, B.; Rossi, M. E.; Kenny, N. J.; Taboada, S.; Koutsouveli, V.; Riesgo, A. Trimitomics: An efficient pipeline for mitochondrial assembly from transcriptomic reads in nonmodel species, Molecular Ecology Resources, Volume 19 (2019) no. 5, pp. 1230-1239 | DOI

[78] R Core Team R: A Language and Environment for Statistical Computing., 2016 (

[79] Reznik, E.; Wang, Q.; La, K.; Schultz, N.; Sander, C. Mitochondrial respiratory gene expression is suppressed in many cancers, eLife, Volume 6 (2017) | DOI

[80] Riesgo, A.; Farrar, N.; Windsor, P. J.; Giribet, G.; Leys, S. P. The Analysis of Eight Transcriptomes from All Poriferan Classes Reveals Surprising Genetic Complexity in Sponges, Molecular Biology and Evolution, Volume 31 (2014) no. 5, pp. 1102-1120 | DOI

[81] RStudio Team RStudio: integrated development for R, 2020 (

[82] Sassaman, C.; Mangum, C. P. Adaptations to environmental oxygen levels in infaunal and epifaunal sea anemones, The Biological Bulletin, Volume 143 (1972) no. 3, pp. 657-678 | DOI

[83] Schmidt O Grundzüge einer Spongien-Fauna des atlantischen Gebietes, Wilhelm Engelmann, 1870, pp. 1-88 (

[84] Schröder, H. C.; Efremova, S. M.; Margulis, B. A.; Guzhova, I. V.; Itskovich, V. B.; Müller, W. E. G. Stress response in Baikalian sponges exposed to pollutants, Hydrobiologia, Volume 568 (2006) no. S1, pp. 277-287 | DOI

[85] Schurch, N. J.; Schofield, P.; Gierliński, M.; Cole, C.; Sherstnev, A.; Singh, V.; Wrobel, N.; Gharbi, K.; Simpson, G. G.; Owen-Hughes, T.; Blaxter, M.; Barton, G. J. How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use?, RNA, Volume 22 (2016) no. 6, pp. 839-851 | DOI

[86] Schuster, A.; Strehlow, B. W.; Eckford-Soper, L.; McAllen, R.; Canfield, D. E. Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland, mSphere, Volume 6 (2021) no. 1 | DOI

[87] Semenza, G. L. Life with Oxygen, Science, Volume 318 (2007) no. 5847, pp. 62-64 | DOI

[88] Simão, F. A.; Waterhouse, R. M.; Ioannidis, P.; Kriventseva, E. V.; Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs, Bioinformatics, Volume 31 (2015) no. 19, pp. 3210-3212 | DOI

[89] Sinha, A.; Sommer, R. J.; Dieterich, C. Divergent gene expression in the conserved dauer stage of the nematodes Pristionchus pacificus and Caenorhabditis elegans, BMC Genomics, Volume 13 (2012) no. 1 | DOI

[90] Sollai, M.; Villanueva, L.; Hopmans, E. C.; Reichart, G.; Sinninghe Damsté, J. S. A combined lipidomic and 16S <scp>rRNA</scp> gene amplicon sequencing approach reveals archaeal sources of intact polar lipids in the stratified Black Sea water column, Geobiology, Volume 17 (2018) no. 1, pp. 91-109 | DOI

[91] Stachowitsch, M. Mass Mortality in the Gulf of Trieste: The Course of Community Destruction, Marine Ecology, Volume 5 (1984) no. 3, pp. 243-264 | DOI

[92] Strader, M. E.; Aglyamova, G. V.; Matz, M. V. Red fluorescence in coral larvae is associated with a diapause‐like state, Molecular Ecology, Volume 25 (2016) no. 2, pp. 559-569 | DOI

[93] Stramma,L ; Johnson, G.; Sprintall, J.; Mohrholz, F. Expanding oxygen-minimum zones in the tropical oceans, Science, Science, Volume 320 (2008), pp. 655-658 | DOI

[94] Strehlow, B. W.; Pineda, M.-C.; Kenkel, C. D.; Laffy, P.; Duckworth, A.; Renton, M.; Clode, P. L.; Webster, N. S. Novel reference transcriptomes for the sponges Carteriospongia foliascens and Cliona orientalis and associated algal symbiont Gerakladium endoclionum | DOI

[95] Strehlow, B. W. Supplemental: Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia, Zenodo, 2024 | DOI

[96] Strehlow, B. W. bstrehlow/Sponge-transcriptomic-responses-to-seasonal-anoxia: v1 (Version v1), Zenodo, 2022 | DOI

[97] Stryer, L. Biochemistry (Fourth ed.), Freeman and Company, New York, 1997, pp. 559-623 (

[98] Topsent, E. Spongiaires de l'Atlantique et de la Méditerranée provenant des croisières du Prince Albert ler de Monaco, Résultats des campagnes scientifiques accomplies par le Prince Albert I, Volume 74 (1928), pp. 1-376 | DOI

[99] Vaquer-Sunyer, R.; Duarte, C. M. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms, Global Change Biology, Volume 17 (2010) no. 5, pp. 1788-1797 | DOI

[100] Vargas, S.; Caglar, C.; Gabi, B.; Schätzle Simone; Deistler Fabian; Gert Wörheide Slime away: a simple {CTAB-based} high molecular weight {DNA} and {RNA} extraction protocol for “difficult” invertebrates,, 2021 | DOI

[101] Webster, N.; Pantile, R.; Botté, E.; Abdo, D.; Andreakis, N.; Whalan, S. A complex life cycle in a warming planet: gene expression in thermally stressed sponges, Molecular Ecology, Volume 22 (2013) no. 7, pp. 1854-1868 | DOI

[102] Webster, N. S.; Taylor, M. W. Marine sponges and their microbial symbionts: love and other relationships, Environmental Microbiology, Volume 14 (2011) no. 2, pp. 335-346 | DOI

[103] Welchen, E.; Gonzalez, D. H. Cytochrome c, a hub linking energy, redox, stress and signaling pathways in mitochondria and other cell compartments, Physiologia Plantarum, Volume 157 (2016) no. 3, pp. 310-321 | DOI

[104] Wilkinson, C. R. Microbial associations in sponges. II. Numerical analysis of sponge and water bacterial populations, Marine Biology, Volume 49 (1978) no. 2, pp. 169-176 | DOI

[105] Wilson, D. F.; Erecińska, M.; Drown, C.; Silver, I. A. The oxygen dependence of cellular energy metabolism, Archives of Biochemistry and Biophysics, Volume 195 (1979) no. 2, pp. 485-493 | DOI

[106] Wright, R. M.; Aglyamova, G. V.; Meyer, E.; Matz, M. V. Gene expression associated with white syndromes in a reef building coral, Acropora hyacinthus, BMC Genomics, Volume 16 (2015) no. 1 | DOI

Cited by Sources: