Lifestyle Evolution in Cyanobacterial Symbionts of Sponges

Burgsdorf, Ilia; Slaby, Beate M.; Handley, Kim M.; Haber, Markus; Blom, Jochen; Marshall, Christopher W.; Gilbert, Jack A.; Hentschel, Ute; Steindler, Laura

doi:10.1128/mBio.00391-15

Title: Lifestyle Evolution in Cyanobacterial Symbionts of Sponges

Journal Article · Tue Jun 02 00:00:00 EDT 2015 · mBio (Online)

DOI:https://doi.org/10.1128/mBio.00391-15· OSTI ID:1214648

Burgsdorf, Ilia ^[1]; Slaby, Beate M. ^[2]; Handley, Kim M. ^[3]; Haber, Markus ^[1]; Blom, Jochen ^[4]; Marshall, Christopher W. ^[5]; Gilbert, Jack A. ^[6]; Hentschel, Ute ^[2]; Steindler, Laura ^[1]

Univ. of Haifa (Israel). Leon H. Charney School of Marine Sciences
Univ. of Würzburg, Würzburg (Germany). Julius-von-Sachs Institute for Biosciences
Univ. of Chicago, IL (United States). Dept. of Ecology and Evolution
Justus-Liebig-Univ. (Germany)
Argonne National Lab. (ANL), Argonne, IL (United States)
Univ. of Chicago, IL (United States). Dept. of Ecology and Evolution; Argonne National Lab. (ANL), Argonne, IL (United States); Marine Biological Lab., Woods Hole, MA (United States of America); Zhejiang Univ. (China). College of Environmental and Resource Sciences

The “Candidatus Synechococcus spongiarum” group includes different clades of cyanobacteria with high 16S rRNA sequence identity (~99%) and is the most abundant and widespread cyanobacterial symbiont of marine sponges. The first draft genome of a “Ca. Synechococcus spongiarum” group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, “Ca. Synechococcus spongiarum” includes a variety of clades that may differ widely in genomic repertoire and consequently in physiology and symbiotic function. Here, we present three additional draft genomes of “Ca. Synechococcus spongiarum,” each from a different clade. By comparing all four symbiont genomes to those of free-living cyanobacteria, we revealed general adaptations to life inside sponges and specific adaptations of each phylotype. Symbiont genomes shared about half of their total number of coding genes. Common traits of “Ca. Synechococcus spongiarum” members were a high abundance of DNA modification and recombination genes and a reduction in genes involved in inorganic ion transport and metabolism, cell wall biogenesis, and signal transduction mechanisms. Moreover, these symbionts were characterized by a reduced number of antioxidant enzymes and low-weight peptides of photosystem II compared to their free-living relatives. Variability within the “Ca. Synechococcus spongiarum” group was mostly related to immune system features, potential for siderophore-mediated iron transport, and dependency on methionine from external sources. The common absence of genes involved in synthesis of residues, typical of the O antigen of free-living Synechococcus species, suggests a novel mechanism utilized by these symbionts to avoid sponge predation and phage attack.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1214648

Journal Information:: mBio (Online), Vol. 6, Issue 3; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 77 works

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Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical Dysideidae Sponges Schorn, Michelle A.; Jordan, Peter A.; Podell, Sheila mBio, Vol. 10, Issue 3 https://doi.org/10.1128/mbio.00821-19	journal	May 2019
Expression of eukaryotic-like protein in the microbiome of sponges Díez-Vives, C.; Moitinho-Silva, L.; Nielsen, S. Molecular Ecology, Vol. 26, Issue 5 https://doi.org/10.1111/mec.14003	journal	January 2017
Phylogeny and genomics of SAUL, an enigmatic bacterial lineage frequently associated with marine sponges: Phylogeny and genomics of SAUL Astudillo-García, Carmen; Slaby, Beate M.; Waite, David W. Environmental Microbiology, Vol. 20, Issue 2 https://doi.org/10.1111/1462-2920.13965	journal	November 2017
Life at Home and on the Roam: Genomic Adaptions Reflect the Dual Lifestyle of an Intracellular, Facultative Symbiont Burgsdorf, Ilia; Handley, Kim M.; Bar-Shalom, Rinat mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/msystems.00057-19	journal	May 2019
The deep-sea glass sponge L ophophysema eversa harbours potential symbionts responsible for the nutrient conversions of carbon, nitrogen and sulfur : Potential symbionts in a glass sponge Tian, Ren-Mao; Sun, Jin; Cai, Lin Environmental Microbiology, Vol. 18, Issue 8 https://doi.org/10.1111/1462-2920.13161	journal	January 2016
Localized production of defence chemicals by intracellular symbionts of Haliclona sponges Tianero, Ma. Diarey; Balaich, Jared N.; Donia, Mohamed S. Nature Microbiology, Vol. 4, Issue 7 https://doi.org/10.1038/s41564-019-0415-8	journal	April 2019
Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts Rubin-Blum, Maxim; Antony, Chakkiath Paul; Sayavedra, Lizbeth The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-019-0346-7	journal	January 2019
BluePharmTrain: Biology and Biotechnology of Marine Sponges Steinert, Georg; Stauffer, Carla Huete; Aas-Valleriani, Nele Grand Challenges in Marine Biotechnology https://doi.org/10.1007/978-3-319-69075-9_13	book	May 2018
Microbial community structure of two freshwater sponges using Illumina MiSeq sequencing revealed high microbial diversity Gaikwad, Swapnil; Shouche, Yogesh S.; Gade, Wasudev N. AMB Express, Vol. 6, Issue 1 https://doi.org/10.1186/s13568-016-0211-2	journal	June 2016
Elevated seawater temperature disrupts the microbiome of an ecologically important bioeroding sponge Ramsby, Blake D.; Hoogenboom, Mia O.; Whalan, Steve Molecular Ecology, Vol. 27, Issue 8 https://doi.org/10.1111/mec.14544	journal	March 2018
Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization Slaby, Beate M.; Hackl, Thomas; Horn, Hannes The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.101	journal	July 2017
Differential Toxicity of Cyanobacteria Isolated from Marine Sponges towards Echinoderms and Crustaceans Regueiras, Ana; Pereira, Sandra; Costa, Maria Toxins, Vol. 10, Issue 7 https://doi.org/10.3390/toxins10070297	journal	July 2018
Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment Baker, Lydia J.; Freed, Lindsay L.; Easson, Cole G. eLife, Vol. 8 https://doi.org/10.7554/elife.47606	journal	October 2019
Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated Thaumarchaeota Zhang, Shan; Song, Weizhi; Wemheuer, Bernd mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/msystems.00288-19	journal	August 2019
Metagenomic analyses uncover the differential effect of azide treatment on bacterial community structure by enriching a specific Cyanobacteria present in a saline-alkaline environmental sample Aguirre-Garrido, José Félix; Martínez-Abarca, Francisco; Montiel-Lugo, Daniel International Microbiology, Vol. 23, Issue 3 https://doi.org/10.1007/s10123-020-00119-z	journal	January 2020
First Record of Microbiomes of Sponges Collected From the Persian Gulf, Using Tag Pyrosequencing Najafi, Akram; Moradinasab, Maryam; Nabipour, Iraj Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01500	journal	July 2018
Keeping it in the family: Coevolution of latrunculid sponges and their dominant bacterial symbionts Matcher, Gwynneth F.; Waterworth, Samantha C.; Walmsley, Tara A. MicrobiologyOpen, Vol. 6, Issue 2 https://doi.org/10.1002/mbo3.417	journal	October 2016
Variations in Microbial Diversity and Metabolite Profiles of the Tropical Marine Sponge Xestospongia muta with Season and Depth Villegas-Plazas, Marcela; Wos-Oxley, Melissa L.; Sanchez, Juan A. Microbial Ecology, Vol. 78, Issue 1 https://doi.org/10.1007/s00248-018-1285-y	journal	November 2018
Characterizing the microbiomes of Antarctic sponges: a functional metagenomic approach Moreno-Pino, Mario; Cristi, Antonia; Gillooly, James F. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57464-2	journal	January 2020
Metagenomic binning reveals versatile nutrient cycling and distinct adaptive features in alphaproteobacterial symbionts of marine sponges Karimi, Elham; Slaby, Beate M.; Soares, André R. FEMS Microbiology Ecology, Vol. 94, Issue 6 https://doi.org/10.1093/femsec/fiy074	journal	April 2018
Microbially mediated nutrient cycles in marine sponges Zhang, Fan; Jonas, Lauren; Lin, Hanzhi FEMS Microbiology Ecology, Vol. 95, Issue 11 https://doi.org/10.1093/femsec/fiz155	journal	October 2019
Evolution and function of eukaryotic-like proteins from sponge symbionts Reynolds, David; Thomas, Torsten Molecular Ecology, Vol. 25, Issue 20 https://doi.org/10.1111/mec.13812	journal	September 2016
Genus-wide comparison of Pseudovibrio bacterial genomes reveal diverse adaptations to different marine invertebrate hosts Alex, Anoop; Antunes, Agostinho PLOS ONE, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pone.0194368	journal	May 2018
An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes Horn, Hannes; Slaby, Beate M.; Jahn, Martin T. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01751	journal	November 2016
Diversity of tryptophan halogenases in sponges of the genus Aplysina Gutleben, Johanna; Koehorst, Jasper J.; McPherson, Kyle FEMS Microbiology Ecology, Vol. 95, Issue 8 https://doi.org/10.1093/femsec/fiz108	journal	July 2019

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