Lifestyle Evolution in Cyanobacterial Symbionts of Sponges
Abstract
The âCandidatus Synechococcus spongiarumâ 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 âCa. Synechococcus spongiarumâ group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, âCa. Synechococcus spongiarumâ 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 âCa. Synechococcus spongiarum,â 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 âCa. Synechococcus spongiarumâ 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 âCa. Synechococcus spongiarumâ group wasmore »
- Authors:
-
- Univ. of Haifa (Israel). Leon H. Charney School of Marine Sciences
- Univ. of WĂŒrzburg, WĂŒrzburg (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
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1214648
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 6; Journal Issue: 3; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Burgsdorf, Ilia, Slaby, Beate M., Handley, Kim M., Haber, Markus, Blom, Jochen, Marshall, Christopher W., Gilbert, Jack A., Hentschel, Ute, and Steindler, Laura. Lifestyle Evolution in Cyanobacterial Symbionts of Sponges. United States: N. p., 2015.
Web. doi:10.1128/mBio.00391-15.
Burgsdorf, Ilia, Slaby, Beate M., Handley, Kim M., Haber, Markus, Blom, Jochen, Marshall, Christopher W., Gilbert, Jack A., Hentschel, Ute, & Steindler, Laura. Lifestyle Evolution in Cyanobacterial Symbionts of Sponges. United States. https://doi.org/10.1128/mBio.00391-15
Burgsdorf, Ilia, Slaby, Beate M., Handley, Kim M., Haber, Markus, Blom, Jochen, Marshall, Christopher W., Gilbert, Jack A., Hentschel, Ute, and Steindler, Laura. Tue .
"Lifestyle Evolution in Cyanobacterial Symbionts of Sponges". United States. https://doi.org/10.1128/mBio.00391-15. https://www.osti.gov/servlets/purl/1214648.
@article{osti_1214648,
title = {Lifestyle Evolution in Cyanobacterial Symbionts of Sponges},
author = {Burgsdorf, Ilia and Slaby, Beate M. and Handley, Kim M. and Haber, Markus and Blom, Jochen and Marshall, Christopher W. and Gilbert, Jack A. and Hentschel, Ute and Steindler, Laura},
abstractNote = {The âCandidatus Synechococcus spongiarumâ 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 âCa. Synechococcus spongiarumâ group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, âCa. Synechococcus spongiarumâ 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 âCa. Synechococcus spongiarum,â 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 âCa. Synechococcus spongiarumâ 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 âCa. Synechococcus spongiarumâ 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.},
doi = {10.1128/mBio.00391-15},
journal = {mBio (Online)},
number = 3,
volume = 6,
place = {United States},
year = {Tue Jun 02 00:00:00 EDT 2015},
month = {Tue Jun 02 00:00:00 EDT 2015}
}
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BluePharmTrain: Biology and Biotechnology of Marine Sponges
book, May 2018
- Steinert, Georg; Stauffer, Carla Huete; Aas-Valleriani, Nele
- Grand Challenges in Marine Biotechnology
Microbial community structure of two freshwater sponges using Illumina MiSeq sequencing revealed high microbial diversity
journal, June 2016
- Gaikwad, Swapnil; Shouche, Yogesh S.; Gade, Wasudev N.
- AMB Express, Vol. 6, Issue 1
Elevated seawater temperature disrupts the microbiome of an ecologically important bioeroding sponge
journal, March 2018
- Ramsby, Blake D.; Hoogenboom, Mia O.; Whalan, Steve
- Molecular Ecology, Vol. 27, Issue 8
Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization
journal, July 2017
- Slaby, Beate M.; Hackl, Thomas; Horn, Hannes
- The ISME Journal, Vol. 11, Issue 11
Differential Toxicity of Cyanobacteria Isolated from Marine Sponges towards Echinoderms and Crustaceans
journal, July 2018
- Regueiras, Ana; Pereira, Sandra; Costa, Maria
- Toxins, Vol. 10, Issue 7
Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment
journal, October 2019
- Baker, Lydia J.; Freed, Lindsay L.; Easson, Cole G.
- eLife, Vol. 8
Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated Thaumarchaeota
journal, August 2019
- Zhang, Shan; Song, Weizhi; Wemheuer, Bernd
- mSystems, Vol. 4, Issue 4
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
journal, January 2020
- Aguirre-Garrido, JosĂ© FĂ©lix; MartĂnez-Abarca, Francisco; Montiel-Lugo, Daniel
- International Microbiology, Vol. 23, Issue 3
First Record of Microbiomes of Sponges Collected From the Persian Gulf, Using Tag Pyrosequencing
journal, July 2018
- Najafi, Akram; Moradinasab, Maryam; Nabipour, Iraj
- Frontiers in Microbiology, Vol. 9
Keeping it in the family: Coevolution of latrunculid sponges and their dominant bacterial symbionts
journal, October 2016
- Matcher, Gwynneth F.; Waterworth, Samantha C.; Walmsley, Tara A.
- MicrobiologyOpen, Vol. 6, Issue 2
Variations in Microbial Diversity and Metabolite Profiles of the Tropical Marine Sponge Xestospongia muta with Season and Depth
journal, November 2018
- Villegas-Plazas, Marcela; Wos-Oxley, Melissa L.; Sanchez, Juan A.
- Microbial Ecology, Vol. 78, Issue 1
Characterizing the microbiomes of Antarctic sponges: a functional metagenomic approach
journal, January 2020
- Moreno-Pino, Mario; Cristi, Antonia; Gillooly, James F.
- Scientific Reports, Vol. 10, Issue 1
Metagenomic binning reveals versatile nutrient cycling and distinct adaptive features in alphaproteobacterial symbionts of marine sponges
journal, April 2018
- Karimi, Elham; Slaby, Beate M.; Soares, André R.
- FEMS Microbiology Ecology, Vol. 94, Issue 6
Microbially mediated nutrient cycles in marine sponges
journal, October 2019
- Zhang, Fan; Jonas, Lauren; Lin, Hanzhi
- FEMS Microbiology Ecology, Vol. 95, Issue 11
Evolution and function of eukaryotic-like proteins from sponge symbionts
journal, September 2016
- Reynolds, David; Thomas, Torsten
- Molecular Ecology, Vol. 25, Issue 20
Genus-wide comparison of Pseudovibrio bacterial genomes reveal diverse adaptations to different marine invertebrate hosts
journal, May 2018
- Alex, Anoop; Antunes, Agostinho
- PLOS ONE, Vol. 13, Issue 5
An Enrichment of CRISPR and Other Defense-Related Features in Marine Sponge-Associated Microbial Metagenomes
journal, November 2016
- Horn, Hannes; Slaby, Beate M.; Jahn, Martin T.
- Frontiers in Microbiology, Vol. 7
Diversity of tryptophan halogenases in sponges of the genus Aplysina
journal, July 2019
- Gutleben, Johanna; Koehorst, Jasper J.; McPherson, Kyle
- FEMS Microbiology Ecology, Vol. 95, Issue 8