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The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis

Journal Article · · BMC Genomics
 [1];  [1];  [1];  [2];  [3];  [4];  [5];  [5];  [6];  [7];  [8];  [8];  [8];  [1]
  1. Harvard Univ., Cambridge, MA (United States). Dept. of Organismic and Evolutionary Biology
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Civil and Environmental Engineering
  3. Polar Research Inst. of China, Shanghai (China). SOA Key Lab. for Polar Science
  4. TNO, Zeist (The Netherlands). Microbiology & Systems Biology Group
  5. Georgia Inst. of Technology, Atlanta, GA (United States). School of Biology
  6. Indiana Univ., Bloomington, IN (United States). Dept. of Biology
  7. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  8. Univ. of California, Davis, CA (United States). Genome Center
Symbioses between chemoautotrophic bacteria and marine invertebrates are rare examples of living systems that are virtually independent of photosynthetic primary production. These associations have evolved multiple times in marine habitats, such as deep-sea hydrothermal vents and reducing sediments, characterized by steep gradients of oxygen and reduced chemicals. Due to difficulties associated with maintaining these symbioses in the laboratory and culturing the symbiotic bacteria, studies of chemosynthetic symbioses rely heavily on culture independent methods. The symbiosis between the coastal bivalve, Solemya velum, and its intracellular symbiont is a model for chemosynthetic symbioses given its accessibility in intertidal environments and the ability to maintain it under laboratory conditions. Here, to better understand this symbiosis, the genome of the S. velum endosymbiont was sequenced. Relative to the genomes of obligate symbiotic bacteria, which commonly undergo erosion and reduction, the S. velum symbiont genome was large (2.7 Mb), GC-rich (51%), and contained a large number (78) of mobile genetic elements. Comparative genomics identified sets of genes specific to the chemosynthetic lifestyle and necessary to sustain the symbiosis. In addition, a number of inferred metabolic pathways and cellular processes, including heterotrophy, branched electron transport, and motility, suggested that besides the ability to function as an endosymbiont, the bacterium may have the capacity to live outside the host. In conclusion, the physiological dexterity indicated by the genome substantially improves our understanding of the genetic and metabolic capabilities of the S. velum symbiont and the breadth of niches the partners may inhabit during their lifecycle.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1407257
Alternate ID(s):
OSTI ID: 1241190
Journal Information:
BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 15; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English

References (125)

Marine Chemosynthetic Symbioses book January 2006
Allochromatium vinosum DsrC: Solution-State NMR Structure, Redox Properties, and Interaction with DsrEFH, a Protein Essential for Purple Sulfur Bacterial Sulfur Oxidation journal October 2008
A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. journal March 1996
Expression of form I and form II Rubisco in chemoautotrophic symbioses: Implications for the interpretation of stable carbon isotope values journal December 1995
Status quo in physiological proteomics of the uncultured Riftia pachyptila endosymbiont journal June 2011
Bacterial Sulfur Globules: Occurrence, Structure and Metabolism book January 2006
Marine Chemosynthetic Symbioses book January 2013
Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve-bacteria symbiosis journal April 1992
Elemental sulfur in the gills of three species of clams containing chemoautotrophic symbiotic bacteria: a possible inorganic energy storage compound journal January 1985
Incorporation and utilization of bacterial lipids in theSolemya velum symbiosis journal June 1991
Getting In or Out: Early Segregation Between Importers and Exporters in the Evolution of ATP-Binding Cassette (ABC) Transporters journal January 1999
Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve-bacteria symbiosis journal April 1992
Elemental sulfur in the gills of three species of clams containing chemoautotrophic symbiotic bacteria: a possible inorganic energy storage compound journal January 1985
Incorporation and utilization of bacterial lipids in theSolemya velum symbiosis journal June 1991
Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes journal November 2010
On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves journal February 2012
Correlations Between Bacterial Ecology and Mobile DNA journal June 2010
Insect endosymbionts: manipulators of insect herbivore trophic interactions? journal May 2010
Reductive genome evolution in chemoautotrophic intracellular symbionts of deep-sea Calyptogena clams journal February 2008
Bacterial endosymbioses in Solemya (Mollusca: Bivalvia)—Model systems for studies of symbiont–host adaptation journal October 2006
Na+-translocating NADH: Quinone oxidoreductase: Progress achieved and prospects of investigations journal February 2005
Ammonium and free amino acids as nitrogen sources for the chemoautotrophic symbiosis Solemya reidi Bernard (Bivalvia : Protobranchia) journal June 1992
Ammonium and free amino acids as nitrogen sources for the chemoautotrophic symbiosis Solemya reidi Bernard (Bivalvia : Protobranchia) journal June 1992
On the origin of mitosing cells journal March 1967
Physiology, morphology, and biochemical composition of Riftia pachyptila at Rose Garden in 1985 journal October 1988
The effect of hydrogen sulfide on the metabolism of Solemya velum and enzymes of sulfide oxidation in gill tissue journal January 1987
The path of Carbon in Photosynthesis journal August 1950
Basic local alignment search tool journal October 1990
Sulfur Metabolism in Phototrophic Sulfur Bacteria book January 2008
The bacterial cytochrome cbb3 oxidases journal April 2004
The past and present of sodium energetics: May the sodium-motive force be with you journal July 2008
Reduced Genome of the Thioautotrophic Intracellular Symbiont in a Deep-Sea Clam, Calyptogena okutanii journal May 2007
A challenge for 21st century molecular biology and biochemistry: what are the causes of obligate autotrophy and methanotrophy? journal June 2004
Purification, crystallization and preliminary crystallographic analysis of a dissimilatory DsrAB sulfite reductase in complex with DsrC journal November 2008
Prokaryotic sulfur oxidation journal June 2005
Identification of Substrate Contact Residues Important for the Allosteric Regulation of Phosphofructokinase from Eschericia coli journal June 2003
Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview journal October 2007
WITHDRAWN: An Evaluation of Modern Pottery from Southern Africa as a Magnetic Recorder journal December 2012
WITHDRAWN: An Evaluation of Modern Pottery from Southern Africa as a Magnetic Recorder journal December 2012
Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats journal March 1983
Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS journal September 2000
Nitrate respiration in the hydrothermal vent tubeworm Riftia pachyptila journal December 1993
Our microbial selves: what ecology can teach us journal July 2011
Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics journal October 2011
Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges journal July 2013
Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont journal August 2013
Horizontal endosymbiont transmission in hydrothermal vent tubeworms journal May 2006
Symbiosis insights through metagenomic analysis of a microbial consortium journal September 2006
Hydrogen is an energy source for hydrothermal vent symbioses journal August 2011
Locating proteins in the cell using TargetP, SignalP and related tools journal April 2007
Evolutionary microbial genomics: insights into bacterial host adaptation journal June 2010
Symbiotic diversity in marine animals: the art of harnessing chemosynthesis journal October 2008
The hydrogenases of Thiocapsa roseopersicina journal February 2005
Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth? journal November 1999
Regulation of expression of terminal oxidases in Paracoccus denitrificans : Regulation of expression of terminal oxidases journal April 2001
Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life journal March 2002
Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use journal April 2012
Immunochemical localization of ribulose-1,5-bisphosphate carboxylase in the symbiont-containing gills of Solemya velum (Bivalvia: Mollusca) journal October 1988
Accelerated evolution and Muller's rachet in endosymbiotic bacteria. journal April 1996
Cospeciation of chemoautotrophic bacteria and deep sea clams journal August 1998
Characterization of α-Ketoglutarate-dependent Taurine Dioxygenase from Escherichia coli journal September 1997
Identifying bacterial genes and endosymbiont DNA with Glimmer journal January 2007
UniRef: comprehensive and non-redundant UniProt reference clusters journal March 2007
Clustal W and Clustal X version 2.0 journal September 2007
Lateral Symbiont Acquisition in a Maternally Transmitted Chemosynthetic Clam Endosymbiosis journal February 2008
Intense Transpositional Activity of Insertion Sequences in an Ancient Obligate Endosymbiont journal June 2008
Evidence for Homologous Recombination in Intracellular Chemosynthetic Clam Symbionts journal March 2009
Lateral Phage Transfer in Obligate Intracellular Bacteria (Wolbachia): Verification from Natural Populations journal November 2009
GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions journal June 2001
ACLAME: A CLAssification of Mobile genetic Elements, update 2010 journal November 2009
ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria journal October 2011
OASIS: an automated program for global investigation of bacterial and archaeal insertion sequences journal August 2012
RefSeq microbial genomes database: new representation and annotation strategy journal December 2013
RefSeq microbial genomes database: new representation and annotation strategy journal March 2015
Accelerated Evolutionary Rate in Sulfur-Oxidizing Endosymbiotic Bacteria Associated with the Mode of Symbiont Transmission journal November 1998
Effect of carbon source availability and growth phase on expression of Corynebacterium glutamicum genes involved in the tricarboxylic acid cycle and glyoxylate bypass journal October 2008
Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense journal March 2003
Integrative analysis of environmental sequences using MEGAN4 journal June 2011
Characterization of a complex chemosensory signal transduction system which controls twitching motility in Pseudomonas aeruginosa: Chemosensory control of twitching motility in P. aeruginosa journal March 2004
Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics journal March 2008
Structure, function and evolution of bacterial ferredoxins journal April 1988
Characterization of the pyrophosphate-dependent 6-phosphofructokinase from Methylococcus capsulatus Bath journal November 2008
Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea journal November 2009
The Calyptogena magnifica Chemoautotrophic Symbiont Genome journal February 2007
Real-Time DNA Sequencing from Single Polymerase Molecules journal January 2009
Metagenome of a Versatile Chemolithoautotroph from Expanding Oceanic Dead Zones journal October 2009
Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis journal February 2010
A Genomic Perspective on Protein Families journal October 1997
A Second Soluble Hox-Type NiFe Enzyme Completes the Hydrogenase Set in Thiocapsa roseopersicina BBS journal June 2010
Genetic Subdivision of Chemosynthetic Endosymbionts of Solemya velum along the Southern New England Coast journal July 2009
CO2 Uptake and Fixation by Endosymbiotic Chemoautotrophs from the Bivalve Solemya velum journal December 2006
Fate of Nitrate Acquired by the Tubeworm Riftia pachyptila journal July 2000
Coupling of Bacterial Endosymbiont and Host Mitochondrial Genomes in the Hydrothermal Vent Clam Calyptogena magnifica journal April 2003
Comparison of the Regulation, Metabolic Functions, and Roles in Virulence of the Glyceraldehyde-3-Phosphate Dehydrogenase Homologues gapA and gapB in Staphylococcus aureus journal September 2010
Formate-Dependent Autotrophic Growth in Sinorhizobium meliloti journal July 2008
Extensive Proliferation of Transposable Elements in Heritable Bacterial Symbionts journal November 2007
Topological Analysis of the Aerobic Membrane-Bound Formate Dehydrogenase of Escherichia coli journal December 1998
Molecular Identification of the Urea Uptake System and Transcriptional Analysis of Urea Transporter- and Urease-Encoding Genes in Corynebacterium glutamicum journal October 2004
Sodium Ion Cycle in Bacterial Pathogens: Evidence from Cross-Genome Comparisons journal September 2001
Genetic Subdivision of Chemosynthetic Endosymbionts of Solemya velum along the Southern New England Coast journal July 2009
CO2 Uptake and Fixation by Endosymbiotic Chemoautotrophs from the Bivalve Solemya velum journal December 2006
Assimilation of Inorganic Nitrogen by Marine Invertebrates and Their Chemoautotrophic and Methanotrophic Symbionts journal June 1994
Phylogenetic diversity of bacterial symbionts of Solemya hosts based on comparative sequence analysis of 16S rRNA genes journal January 1997
Coupling of Bacterial Endosymbiont and Host Mitochondrial Genomes in the Hydrothermal Vent Clam Calyptogena magnifica journal April 2003
Developmental fate of Rhizobium meliloti bacteroids in alfalfa nodules journal September 1980
Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis journal May 1992
Isolation and characterization of the Escherichia coli msbB gene, a multicopy suppressor of null mutations in the high-temperature requirement gene htrB journal February 1992
Genomics and Evolution of Heritable Bacterial Symbionts journal December 2008
[NiFe]-Hydrogenases of Ralstonia eutropha H16: Modular Enzymes for Oxygen-Tolerant Biological Hydrogen Oxidation journal January 2005
Detection of gene pathways with predictive power for breast cancer prognosis journal January 2010
GuiTope: an application for mapping random-sequence peptides to protein sequences journal January 2012
Comparative genomics of vesicomyid clam (Bivalvia: Mollusca) chemosynthetic symbionts journal January 2008
The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities journal December 2010
Pathways of inorganic nitrogen assimilation in chemoautotrophic bacteria–marine invertebrate symbioses: expression of host and symbiont glutamine synthetase journal February 1999
Nitrogen Metabolites and Related Enzymatic Activities in the Body Fluids and Tissues of the Hydrothermal Vent Tubeworm Riftia Pachyptila journal October 2000
Phylogenomics of the Reproductive Parasite Wolbachia pipientis wMel: A Streamlined Genome Overrun by Mobile Genetic Elements journal March 2004
Insights into the Genome of Large Sulfur Bacteria Revealed by Analysis of Single Filaments journal August 2007
One Bacterial Cell, One Complete Genome journal April 2010
Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology journal November 2012
Vertical Transmission of Chemoautotrophic Symbionts in the Bivalve Solemya velum (Bivalvia: Protobranchia) journal April 1996
Possible Roles of Sulfur-Containing Amino Acids in a Chemoautotrophic Bacterium-Mollusc Symbiosis journal December 2003
Suspension feeding on phytoplankton by Solemya velum, a symbiont-containing clam journal January 1992
Gradients in dimethylsulfide, dimethylsulfoniopropionate, dimethylsulfoxide, and bacteria near the sea surface journal January 2005
Metatranscriptomic Analysis of Sulfur Oxidation Genes in the Endosymbiont of Solemya Velum journal January 2011
The role of endosymbiotic bacteria in the nutrition of Solemya velum: Evidence from a stable isotope analysis of endosymbionts and host journal January 1989

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