Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

A novel Chromatiales bacterium is a potential sulfide oxidizer in multiple orders of marine sponges

Journal Article · · Environmental Microbiology
 [1];  [1];  [2];  [2];  [2];  [2];  [3]
  1. Tel-Aviv Univ., Tel-Aviv (Israel); Univ. of California, Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States)
  3. Tel-Aviv Univ., Tel-Aviv (Israel)

Here, sponges are benthic filter feeders that play pivotal roles in coupling benthic-pelagic processes in the oceans that involve transformation of dissolved and particulate organic carbon and nitrogen into biomass. While the contribution of sponge holobionts to the nitrogen cycle has been recognized in past years, their importance in the sulfur cycle, both oceanic and physiological, has only recently gained attention. Sponges in general, and Theonella swinhoei in particular, harbour a multitude of associated microorganisms that could affect sulfur cycling within the holobiont. We reconstructed the genome of a Chromatiales (class Gammaproteobacteria) bacterium from a metagenomic sequence dataset of a T. swinhoei-associated microbial community. This relatively abundant bacterium has the metabolic capability to oxidize sulfide yet displays reduced metabolic potential suggestive of its lifestyle as an obligatory symbiont. This bacterium was detected in multiple sponge orders, according to similarities in key genes such as 16S rRNA and polyketide synthase genes. Due to its sulfide oxidation metabolism and occurrence in many members of the Porifera phylum, we suggest naming the newly described taxon Candidatus Porisulfidus.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1479381
Alternate ID(s):
OSTI ID: 1420453
Journal Information:
Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 2 Vol. 20; ISSN 1462-2912
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (88)

Two classes of metabolites fromTheonella swinhoei are localized in distinct populations of bacterial symbionts journal July 1996
Marine sponges as habitats of anaerobic phototrophic bacteria journal March 1976
Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes journal August 2006
Oxygen dynamics and transport in the Mediterranean sponge Aplysina aerophoba journal January 2008
Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel δ-proteobacterium, " Candidatus Entotheonella palauensis" journal July 2000
Phylogenetic Diversity and Spatial Distribution of the Microbial Community Associated with the Caribbean Deep-water Sponge Polymastia cf. corticata by 16S rRNA, aprA, and amoA Gene Analysis journal January 2008
Increasing the Richness of Culturable Arsenic-Tolerant Bacteria from Theonella swinhoei by Addition of Sponge Skeleton to the Growth Medium journal January 2016
Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? journal November 2007
A case study on chemical defense based on quorum sensing: antibacterial activity of sponge-associated bacterium Pseudoalteromonas sp. NJ6-3-1 induced by quorum sensing mechanisms journal September 2010
Study of seawater alkalization as a promising RO pretreatment method journal February 2003
Lifestyle evolution in symbiotic bacteria: insights from genomics journal August 2000
The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism journal July 2014
Sulfur-oxidizing bacteria in environmental technology journal November 2015
Chemosynthetic endosymbioses: adaptations to oxic–anoxic interfaces journal September 2005
Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? journal March 2010
Nagahamide A, an Antibacterial Depsipeptide from the Marine Sponge Theonella swinhoei 1 journal September 2002
Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges journal July 2009
Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges journal October 2011
‘Sponge-specific’ bacteria are widespread (but rare) in diverse marine environments journal October 2012
Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont journal August 2013
Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases journal October 2014
Ecophysiology of Thioploca ingrica as revealed by the complete genome sequence supplemented with proteomic evidence journal October 2014
Uncultivated microbes in need of their own taxonomy journal July 2017
Integrated metabolism in sponge–microbe symbiosis revealed by genome-centered metatranscriptomics journal March 2017
An environmental bacterial taxon with a large and distinct metabolic repertoire journal January 2014
Unusual biology across a group comprising more than 15% of domain Bacteria journal June 2015
Calyculin biogenesis from a pyrophosphate protoxin produced by a sponge symbiont journal June 2014
Diversity, structure and convergent evolution of the global sponge microbiome journal June 2016
Sponge-associated bacteria mineralize arsenic and barium on intracellular vesicles journal February 2017
Fast gapped-read alignment with Bowtie 2 journal March 2012
Metabolites from symbiotic bacteria journal January 2009
Metabolites from symbiotic bacteriaThis review is dedicated to Professor Axel Zeeck on the occasion of his 65th birthday. journal January 2004
Taxonomy, reproduction and ecology of new and known Red Sea sponges journal December 2004
Oxygen dynamics in choanosomal sponge explants journal May 2005
Studies on the Metabolism of Autotrophic Bacteria: i. the Respiration of Thiobacillus Thiooxidans on Sulfur journal September 1942
The HMA-LMA Dichotomy Revisited: an Electron Microscopical Survey of 56 Sponge Species journal August 2014
Profile hidden Markov models journal October 1998
Search and clustering orders of magnitude faster than BLAST journal August 2010
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth journal April 2012
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data journal April 2012
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
KAAS: an automatic genome annotation and pathway reconstruction server journal May 2007
HMMER web server: 2015 update journal May 2015
antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters journal May 2015
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees journal April 2016
IMG/M: integrated genome and metagenome comparative data analysis system journal October 2016
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 journal March 2010
DNA–DNA hybridization values and their relationship to whole-genome sequence similarities journal January 2007
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates journal January 2017
Genomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur-oxidizing bacterium in sponge: A versatile SOB as a potential sponge symbiont journal August 2014
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 journal January 2016
Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO 2 concentrations : Genomic resolution of a high-CO journal July 2016
Habitat- and host-related variation in sponge bacterial symbiont communities in Indonesian waters journal May 2013
Implementing sponge physiological and genomic information to enhance the diversity of its culturable associated bacteria journal December 2013
Lucinidae (Bivalvia)–the most diverse group of chemosymbiotic molluscs journal November 2006
Complex nitrogen cycling in the sponge Geodia barretti journal September 2009
Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms: Sponge-associated microorganisms journal December 2011
Comparison of prokaryotic diversity at offshore oceanic locations reveals a different microbiota in the Mediterranean Sea: Offshore prokaryotic diversity journal June 2006
Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea journal November 2009
Diversity of Bacteria in the Marine Sponge Aplysina fulva in Brazilian Coastal Waters journal March 2009
Oxidation of Reduced Inorganic Sulfur Compounds by Bacteria: Emergence of a Common Mechanism? journal July 2001
Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential journal June 2007
The Sponge Hologenome journal April 2016
Genome Reduction and Microbe-Host Interactions Drive Adaptation of a Sulfur-Oxidizing Bacterium Associated with a Cold Seep Sponge journal March 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling journal January 2013
Community-wide analysis of microbial genome sequence signatures journal January 2009
Proposal for a revised classification of the Demospongiae (Porifera) journal April 2015
Pyrosequencing of Bacterial Symbionts within Axinella corrugata Sponges: Diversity and Seasonal Variability journal June 2012
Phylogenetically and Spatially Close Marine Sponges Harbour Divergent Bacterial Communities journal December 2012
Phylogenetically Diverse ureC Genes and Their Expression Suggest the Urea Utilization by Bacterial Symbionts in Marine Sponge Xestospongia testudinaria journal May 2013
Evidence of a Putative Deep Sea Specific Microbiome in Marine Sponges journal March 2014
Environmental Assessment of the Gulf of Aqaba Coastal Surface Waters, Saudi Arabia journal March 2014
Endobionts of the Coral Reef Sponge Theonella swinhoei (Porifera, Demospongiae) journal July 1999
Draft Genomes Shed Light on the Dual Bacterial Symbiosis that Dominates the Microbiome of the Coral Reef Sponge Amphimedon queenslandica journal October 2016
Intermittent Hypoxia and Prolonged Suboxia Measured In situ in a Marine Sponge journal December 2016
Culturable associated-bacteria of the sponge Theonella swinhoei show tolerance to high arsenic concentrations journal February 2015
Predicting the HMA-LMA Status in Marine Sponges by Machine Learning journal May 2017
Sponge-Specific Unknown Bacterial Groups Detected in Marine Sponges Collected from Korea Through Barcoded Pyrosequencing journal January 2015
Complete genome sequence of Thioalkalivibrio “sulfidophilus” HL-EbGr7 journal February 2011
Complete genome sequence of Thioalkalivibrio sp. K90mix journal December 2011
Microbial transformations of sulfur compounds in a stratified lake (Solar Lake, Sinai)1: Sulfur cycle in a stratified lake journal September 1979
In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei : Bulk DOC is the major source for carbon journal January 2003
In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida journal May 2008
Heterogeneous oxygenation resulting from active and passive flow in two Mediterranean sponges, Dysida avara and Chondrosia reniformis journal April 2010
In four shallow and mesophotic tropical reef sponges from Guam the microbial community largely depends on host identity journal January 2016

Cited By (2)

Microbially mediated nutrient cycles in marine sponges journal October 2019
Cultivation of Sponge-Associated Bacteria from Agelas sventres and Xestospongia muta Collected from Different Depths journal October 2019

Similar Records

Genomics of "Candidatus Synechococcus spongiarium", a Cyanobacterial Sponge Symbiont
Conference · Fri Mar 21 00:00:00 EDT 2014 · OSTI ID:1241192

Lifestyle Evolution in Cyanobacterial Symbionts of Sponges
Journal Article · Tue Jun 02 00:00:00 EDT 2015 · mBio (Online) · OSTI ID:1214648

Complete genome sequence of Candidatus Ruthia magnifica
Journal Article · Wed Oct 27 00:00:00 EDT 2010 · Standards in Genomic Sciences · OSTI ID:1628649

Related Subjects