Microbiome of the freshwater sponge Ephydatia muelleri shares compositional and functional similarities with those of marine sponges
Yin Z, Zhu M, Davidson EH, Bottjer DJ, Zhao F, Tafforeau P. Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc Natl Acad Sci. 2015;112:E1453–E1460.
Google Scholar
Webster NS, Thomas T. The sponge hologenome. MBio. 2016;7:e00135–16.
Google Scholar
Hentschel U, Piel J, Degnan SM, Taylor MW. Genomic insights into the marine sponge microbiome. Nat Rev Microbiol. 2012;10:641–54.
Google Scholar
van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K, de Voogd NJ, Alvarez B, et al. World Porifera Database. http://www.marinespecies.org/porifera.
Laport MS, Pinheiro U, da Costa Rachid CTC. Freshwater sponge Tubella variabilis presents richer microbiota than marine sponge species. Front Microbiol. 2019;10:2799.
Google Scholar
Manconi R, Pronzato R. Global diversity of sponges (Porifera: Spongillina) in freshwater. Hydrobiologia. 2008;595:27–33.
Google Scholar
Gladkikh AS, Kalyuzhnaya OV, Belykh OI, Ahn TS, Parfenova VV. Analysis of bacterial communities of two Lake Baikal endemic sponge species. Microbiology. 2014;83:787–97.
Google Scholar
Kulakova NV, Sakirko MV, Adelshin RV, Khanaev IV, Nebesnykh IA, Pérez T. Brown rot syndrome and changes in the bacterial community of the Baikal sponge Lubomirskia baicalensis. Micro Ecol. 2018;75:1024–34.
Google Scholar
Kaluzhnaya O, Krivich A, Itskovich V. Diversity of 16S rRNA genes in metagenomic community of the freshwater sponge Lubomirskia baicalensis. Russ J Genet. 2012;48:855–8.
Google Scholar
Parfenova V, Terkina I, Kostornova TY, Nikulina IG, Chernykh VI, Maksimova EA. Microbial community of freshwater sponges in Lake Baikal. Biol Bull. 2008;35:374–9.
Google Scholar
Belikov S, Belkova N, Butina T, Chernogor L, Kley AM, Nalian A, et al. Diversity and shifts of the bacterial community associated with Baikal sponge mass mortalities. PLoS One. 2019;14:e0213926.
Google Scholar
Petrushin I, Belikov S, Chernogor L. Cooperative interaction of Janthinobacterium sp. Slb01 and Flavobacterium sp. slb02 in the diseased sponge Lubomirskia baicalensis. Int J Mol Sci. 2020;21:8128.
Google Scholar
Chernogor L, Klimenko E, Khanaev I, Belikov S. Microbiome analysis of healthy and diseased sponges Lubomirskia baicalensis by using cell cultures of primmorphs. PeerJ. 2020;8:e9080.
Google Scholar
Wilkinson CR. Nutrient translocation from green algal symbionts to the freshwater sponge Ephydatia fluviatilis. Hydrobiologia. 1980;75:241–50.
Google Scholar
Costa R, Keller-Costa T, Gomes NCM, da Rocha UN, van Overbeek L, van Elsas JD. Evidence for selective bacterial community structuring in the freshwater sponge Ephydatia fluviatilis. Micro Ecol. 2013;65:232–44.
Google Scholar
Keller-Costa T, Jousset A, Van Overbeek L, Van Elsas JD, Costa R. The freshwater sponge Ephydatia fluviatilis harbours diverse Pseudomonas species (Gammaproteobacteria, Pseudomonadales) with broad-spectrum antimicrobial activity. PLoS One. 2014;9:e88429.
Google Scholar
Kenny NJ, Francis WR, Rivera-Vicéns RE, Juravel K, de Mendoza A, Díez-Vives C, et al. Tracing animal genomic evolution with the chromosomal-level assembly of the freshwater sponge Ephydatia muelleri. Nat Commun. 2020;11:3676.
Google Scholar
Frost TM, Williamson CE. In situ determination of the effect of symbiotic algae on the growth of the fresh water sponge Spongilla lacustris. Ecology. 1980;61:1361–70.
Google Scholar
Gernert C, Glöckner FO, Krohne G, Hentschel U. Microbial diversity of the freshwater sponge Spongilla lacustris. Micro Ecol. 2005;50:206–12.
Google Scholar
Gaikwad S, Shouche YS, Gade WN. Microbial community structure of two freshwater sponges using Illumina MiSeq sequencing revealed high microbial diversity. AMB Express. 2016;6:40.
Google Scholar
Rozas EE, Mendes MA, Nascimento CAO, Rodrigues JCV, Albano RM, Custódio MR. Reduction of RBL–2H3 cells degranulation by nitroaromatic compounds from a Bacillus strain associated to the Amazonian sponge Metania reticulata. J Mar Biol Assoc U Kingd. 2016;96:567–72.
Google Scholar
Marino CM, Pawlik JR, López-Legentil S, Erwin PM. Latitudinal variation in the microbiome of the sponge Ircinia campana correlates with host haplotype but not anti-predatory chemical defense. Mar Ecol Prog Ser. 2017;565:53–66.
Google Scholar
Griffiths SM, Antwis RE, Lenzi L, Lucaci A, Behringer DC, Butler MJ, et al. Host genetics and geography influence microbiome composition in the sponge Ircinia campana. J Anim Ecol. 2019;88:1684–95.
Google Scholar
Easson CG, Chaves-Fonnegra A, Thacker RW, Lopez JV. Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix. Ecol Evol. 2020;10:2007–20.
Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, et al. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci. 2012;109:E1878–E1887.
Google Scholar
Díez-Vives C, Esteves AIS, Costa R, Nielsen S, Thomas T. Detecting signatures of a sponge-associated lifestyle in bacterial genomes. Environ Microbiol Rep. 2018;10:433–43.
Google Scholar
Engelberts JP, Robbins SJ, de Goeij JM, Aranda M, Bell SC, Webster NS. Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J. 2020;14:1100–10.
Google Scholar
Zhang F, Jonas L, Lin H, Hill RT. Microbially mediated nutrient cycles in marine sponges. FEMS Microbiol Ecol. 2019;95:fiz155.
Google Scholar
Horn H, Slaby BM, Jahn MT, Bayer K, Moitinho-Silva L, Förster F, et al. An enrichment of CRISPR and other defense-related features in marine sponge-associated microbial metagenomes. Front Microbiol. 2016;7:1751.
Google Scholar
Díez-Vives C, Moitinho-Silva L, Nielsen S, Reynolds D, Thomas T. Expression of eukaryotic-like protein in the microbiome of sponges. Mol Ecol. 2017;26:1432–51.
Google Scholar
Nguyen MTHD, Liu M, Thomas T. Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis. Mol Ecol. 2014;23:1635–45.
Google Scholar
Moore D, Dowhan D. Purification and concentration of DNA from aqueous solutions. Curr Protoc Mol Biol. 2002;59:2.1.1–2.1.10.
Caporaso JG, Lauber CL, Walters WA, Berg-lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci. 2011;108:4516–22.
Google Scholar
Sugden SA, St. Clair CC, Stein LY. Individual and site-specific variation in a biogeographical profile of the coyote intestinal microbiota. Micro Ecol. 2021;81:240–52.
Google Scholar
Callahan BJ, Mcmurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
Google Scholar
McMurdie PJ, Holmes S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8:e61217.
Google Scholar
Li D, Luo R, Liu C-M, Leung C-M, Ting H-F, Sadakane K, et al. MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11.
Google Scholar
Tatusov RL, Galperin MY, Natale DA, Koonin E. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28:33–36.
Google Scholar
R Core Team. R: A language and environment for statistical computing. 2019. Vienna, Austria.
Hsieh TC, Ma KH, Chao A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol. 2016;7:1451–6.
Google Scholar
Fernandes AD, Reid JNS, Macklaim JM, McMurrough TA, Edgell DR, Gloor GB, et al. Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome. 2014;2:15.
Google Scholar
Epstein HE, Hernandez-Agreda A, Starko S, Baum JK, Vega Thurber R. Inconsistent patterns of microbial diversity and composition between highly similar sequencing protocols: a case study with reef-building corals. Front Microbiol. 2021;12:3585.
Google Scholar
Corcoll N, Österlund T, Sinclair L, Eiler A, Kristiansson E, Backhaus T, et al. Comparison of four DNA extraction methods for comprehensive assessment of 16S rRNA bacterial diversity in marine biofilms using high-throughput sequencing. FEMS Microbiol Lett. 2017;364:fnx139.
Google Scholar
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.
Google Scholar
Francis WR, Eitel M, Vargas S, Krebs S, Blum H, Wörheide G. Mitochondrial genomes of the freshwater sponges Spongilla lacustris and Ephydatia cf. muelleri. Mitochondrial DNA Part B Resour. 2016;1:250–1.
Google Scholar
Rosenberg E. The Family Chitinophagaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, (eds). The Prokaryotes: Other Major Lineages of Bacteria and The Archaea. Berlin, Heidelberg: Springer; 2014. p. 493–5.
Bergstrand LH, Cardenas E, Holert J, van Hamme JD, Mohn WW. Delineation of steroid-degrading microorganisms through comparative genomic analysis. MBio. 2016;7:e00166–16.
Google Scholar
Nelson WC, Tully BJ, Mobberley JM. Biases in genome reconstruction from metagenomic data. PeerJ. 2020;8:e10119.
Google Scholar
Moitinho-Silva L, Nielsen S, Amir A, Gonzalez A, Ackermann GL, Cerrano C, et al. The sponge microbiome project. Gigascience. 2017;6:gix077.
Google Scholar
Hardoim CCP, Costa R, Araújo FV, Hajdu E, Peixoto R, Lins U, et al. Diversity of bacteria in the marine sponge Aplysina fulva in Brazilian coastal waters. Appl Environ Microbiol. 2009;75:3331–43.
Google Scholar
Souza DT, Genuario DB, Silva FSP, Pansa CC, Kavamura VN, Moraes FC, et al. Analysis of bacterial composition in marine sponges reveals the influence of host phylogeny and environment. FEMS Microbiol Ecol. 2017;93:fiw204.
Google Scholar
Slaby BM, Hackl T, Horn H, Bayer K, Hentschel U. Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization. ISME J. 2017;11:2465–78.
Google Scholar
Wysokowski M, Petrenko I, Stelling AL, Stawski D, Jesionowski T, Ehrlich H. Poriferan chitin as a versatile template for extreme biomimetics. Polym (Basel). 2015;7:235–65.
Google Scholar
Ehrlich H, Kaluzhnaya OV, Brunner E, Tsurkan MV, Ereskovsky A, Ilan M, et al. Identification and first insights into the structure and biosynthesis of chitin from the freshwater sponge Spongilla lacustris. J Structual Biol. 2013;183:474–83.
Google Scholar
Liu L, Zhu W, Cao Z, Xu B, Wang G, Luo M. High correlation between genotypes and phenotypes of environmental bacteria Comamonas testosteroni strains. BMC Genomics. 2015;16:110.
Google Scholar
Rix L, de Goeij JM, van Oevelen D, Struck U, Al-Horani FA, Wild C, et al. Differential recycling of coral and algal dissolved organic matter via the sponge loop. Funct Ecol. 2017;31:778–89.
Google Scholar
Robbins SJ, Song W, Engelberts JP, Glasl B, Slaby BM, Boyd J, et al. A genomic view of the microbiome of coral reef demosponges. ISME J. 2021;15:1641–54.
Google Scholar
Karimi E, Slaby BM, Soares AR, Blom J, Hentschel U, Costa R. Metagenomic binning reveals versatile nutrient cycling and distinct adaptive features in alphaproteobacterial symbionts of marine sponges. FEMS Microbiol Ecol. 2018;94:fiy074.
Google Scholar
Luter HM, Widder S, Botté ES, Abdul Wahab M, Whalan S, Moitinho-Silva L, et al. Biogeographic variation in the microbiome of the ecologically important sponge, Carteriospongia foliascens. PeerJ. 2015;3:e1435.
Google Scholar
Luter HM, Whalan S, Webster NS. Thermal and sedimentation stress are unlikely causes of brown spot syndrome in the coral reef sponge, Ianthella basta. PLoS One. 2012;7:e39779.
Google Scholar
Simister R, Taylor MW, Rogers KM, Schupp PJ, Deines P. Temporal molecular and isotopic analysis of active bacterial communities in two New Zealand sponges. FEMS Microbiol Ecol. 2013;85:195–205.
Google Scholar
Thinesh T, Meenatchi R, Pasiyappazham R, Jose PA, Selvan M, Kiran GS, et al. Short-term in situ shading effectively mitigates linear progression of coral-killing sponge Terpios hoshinota. PLoS One. 2017;12:e0182365.
Google Scholar
Ribes M, Calvo E, Movilla J, Logares R, Coma R, Pelejero C. Restructuring of the sponge microbiome favors tolerance to ocean acidification. Environ Microbiol Rep. 2016;8:536–44.
Google Scholar
de Oliveira BFR, Freitas-Silva J, Sánchez-Robinet C, Laport MS. Transmission of the sponge microbiome: moving towards a unified model. Environ Microbiol Rep. 2020;12:619–38.
Google Scholar
Ebert D. The epidemiology and evolution of symbionts with mixed-mode transmission. Annu Rev Ecol Evol Syst. 2013;44:623–43.
Google Scholar
Wu S, Ou H, Liu T, Wang D, Zhao J. Structure and dynamics of microbiomes associated with the marine sponge Tedania sp. during its life cycle. FEMS Microbiol Ecol. 2018;94:fiy055.
Google Scholar
Oliveira BFR, Lopes IR, Canellas ALB, Muricy G, Dobson ADW, Laport MS. Not that close to mommy: horizontal transmission seeds the microbiome associated with the marine sponge plakina cyanorosea. Microorganisms. 2020;8:1978.
Google Scholar
Gloeckner V, Lindquist N, Schmitt S, Hentschel U. Ectyoplasia ferox, an experimentally tractable model for vertical microbial transmission in marine sponges. Micro Ecol. 2013;65:462–74.
Google Scholar
Simpson TL, Gilbert JJ. Gemmulation, gemmule hatching, and sexual reproduction in fresh-water sponges – I. The life cycle of Spongilla lacustris and Tubella pennsylvanica. Trans Am Microsc Soc. 1973;92:422–33.
Google Scholar
Karimi E, Keller-Costa T, Slaby BM, Cox CJ, da Rocha UN, Hentschel U, et al. Genomic blueprints of sponge-prokaryote symbiosis are shared by low abundant and cultivatable Alphaproteobacteria. Sci Rep. 2019;9:1999.
Google Scholar
Karimi E, Ramos M, Gonçalves JMS, Xavier JR, Reis MP, Costa R. Comparative metagenomics reveals the distinctive adaptive features of the Spongia officinalis endosymbiotic consortium. Front Microbiol. 2017;8:2499.
Google Scholar
Cardoso JFMF, Van Bleijswijk JDL, Witte H, Van Duyl FC. Diversity and abundance of ammonia-oxidizing Archaea and Bacteria in tropical and cold-water coral reef sponges. Aquat Microb Ecol. 2013;68:215–30.
Schläppy ML, Schöttner SI, Lavik G, Kuypers MMM, de Beer D, Hoffmann F. Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol. 2010;157:593–602.
Google Scholar
Bayer K, Moitinho-Silva L, Brümmer F, Cannistraci CV, Ravasi T, Hentschel U. GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater. FEMS Microbiol Ecol. 2014;90:832–43.
Google Scholar
Tanaka Y, Miyajima T, Watanabe A, Nadaoka K, Yamamoto T, Ogawa H. Distribution of dissolved organic carbon and nitrogen in a coral reef. Coral Reefs. 2011;30:533–41.
Google Scholar
Simister R, Taylor MW, Tsai P, Webster NS. Sponge-microbe associations survive high nutrients and temperatures. PLoS One. 2012;7:e52220.
Google Scholar
Bayer K, Busch K, Kenchington E, Beazley L, Franzenburg S, Michels J, et al. Microbial strategies for survival in the glass sponge Vazella pourtalesii. mSystems. 2020;5:e00473–20.
Google Scholar
Phelan RW, O’Halloran JA, Kennedy J, Morrissey JP, Dobson ADW, O’Gara F, et al. Diversity and bioactive potential of endospore-forming bacteria cultured from the marine sponge Haliclona simulans. J Appl Microbiol. 2012;112:65–78.
Google Scholar