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

Abstract

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 anmore » 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.« less

Authors:
 [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
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1407257
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 15; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Symbiosis; Chemosynthesis; Sulfur oxidation; Respiratory flexibility; H+/Na+ -membrane cycles; Calvin cycle; Pyrophosphate-dependent phosphofructokinase; Heterotrophy; Motility; Mobile genetic elements

Citation Formats

Dmytrenko, Oleg, Russell, Shelbi L., Loo, Wesley T., Fontanez, Kristina M., Liao, Li, Roeselers, Guus, Sharma, Raghav, Stewart, Frank J., Newton, Irene LG, Woyke, Tanja, Wu, Dongying, Lang, Jenna, Eisen, Jonathan A., and Cavanaugh, Colleen M. The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis. United States: N. p., 2014. Web. doi:10.1186/1471-2164-15-924.
Dmytrenko, Oleg, Russell, Shelbi L., Loo, Wesley T., Fontanez, Kristina M., Liao, Li, Roeselers, Guus, Sharma, Raghav, Stewart, Frank J., Newton, Irene LG, Woyke, Tanja, Wu, Dongying, Lang, Jenna, Eisen, Jonathan A., & Cavanaugh, Colleen M. The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis. United States. https://doi.org/10.1186/1471-2164-15-924
Dmytrenko, Oleg, Russell, Shelbi L., Loo, Wesley T., Fontanez, Kristina M., Liao, Li, Roeselers, Guus, Sharma, Raghav, Stewart, Frank J., Newton, Irene LG, Woyke, Tanja, Wu, Dongying, Lang, Jenna, Eisen, Jonathan A., and Cavanaugh, Colleen M. Thu . "The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis". United States. https://doi.org/10.1186/1471-2164-15-924. https://www.osti.gov/servlets/purl/1407257.
@article{osti_1407257,
title = {The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis},
author = {Dmytrenko, Oleg and Russell, Shelbi L. and Loo, Wesley T. and Fontanez, Kristina M. and Liao, Li and Roeselers, Guus and Sharma, Raghav and Stewart, Frank J. and Newton, Irene LG and Woyke, Tanja and Wu, Dongying and Lang, Jenna and Eisen, Jonathan A. and Cavanaugh, Colleen M.},
abstractNote = {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.},
doi = {10.1186/1471-2164-15-924},
journal = {BMC Genomics},
number = 1,
volume = 15,
place = {United States},
year = {Thu Oct 23 00:00:00 EDT 2014},
month = {Thu Oct 23 00:00:00 EDT 2014}
}

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Works referenced in this record:

Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis
journal, February 2010


Genetic Subdivision of Chemosynthetic Endosymbionts of Solemya velum along the Southern New England Coast
journal, July 2009

  • Stewart, Frank J.; Baik, Alan Hyun Y.; Cavanaugh, Colleen M.
  • Applied and Environmental Microbiology, Vol. 75, Issue 18
  • DOI: 10.1128/aem.00689-09

Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes
journal, November 2010

  • Biegel, Eva; Schmidt, Silke; González, José M.
  • Cellular and Molecular Life Sciences, Vol. 68, Issue 4
  • DOI: 10.1007/s00018-010-0555-8

Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense
journal, March 2003

  • Nunoura, Takuro; Sako, Yoshihiko; Wakagi, Takayoshi
  • Microbiology, Vol. 149, Issue 3
  • DOI: 10.1099/mic.0.26000-0

Comparative genomics of vesicomyid clam (Bivalvia: Mollusca) chemosynthetic symbionts
journal, January 2008

  • Newton, Irene LG; Girguis, Peter R.; Cavanaugh, Colleen M.
  • BMC Genomics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2164-9-585

Evidence for Homologous Recombination in Intracellular Chemosynthetic Clam Symbionts
journal, March 2009

  • Stewart, F. J.; Young, C. R.; Cavanaugh, C. M.
  • Molecular Biology and Evolution, Vol. 26, Issue 6
  • DOI: 10.1093/molbev/msp049

Fate of Nitrate Acquired by the Tubeworm Riftia pachyptila
journal, July 2000


The effect of hydrogen sulfide on the metabolism of Solemya velum and enzymes of sulfide oxidation in gill tissue
journal, January 1987

  • Chen, Chong; Rabourdin, Bruno; Hammen, C. S.
  • Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Vol. 88, Issue 3
  • DOI: 10.1016/0305-0491(87)90269-0

Coupling of Bacterial Endosymbiont and Host Mitochondrial Genomes in the Hydrothermal Vent Clam Calyptogena magnifica
journal, April 2003


Symbiotic diversity in marine animals: the art of harnessing chemosynthesis
journal, October 2008

  • Dubilier, Nicole; Bergin, Claudia; Lott, Christian
  • Nature Reviews Microbiology, Vol. 6, Issue 10
  • DOI: 10.1038/nrmicro1992

Accelerated Evolutionary Rate in Sulfur-Oxidizing Endosymbiotic Bacteria Associated with the Mode of Symbiont Transmission
journal, November 1998


Purification, crystallization and preliminary crystallographic analysis of a dissimilatory DsrAB sulfite reductase in complex with DsrC
journal, November 2008

  • Oliveira, Tânia F.; Vonrhein, Clemens; Matias, Pedro M.
  • Journal of Structural Biology, Vol. 164, Issue 2
  • DOI: 10.1016/j.jsb.2008.07.007

Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life
journal, March 2002

  • Gil, R.; Sabater-Munoz, B.; Latorre, A.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 7
  • DOI: 10.1073/pnas.062067299

Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve-bacteria symbiosis
journal, April 1992

  • Conway, Noellette M.; Howes, Brain L.; McDowell Capuzzo, Judith E.
  • Marine Biology, Vol. 112, Issue 4
  • DOI: 10.1007/bf00346178

The past and present of sodium energetics: May the sodium-motive force be with you
journal, July 2008

  • Mulkidjanian, Armen Y.; Dibrov, Pavel; Galperin, Michael Y.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 7-8
  • DOI: 10.1016/j.bbabio.2008.04.028

[NiFe]-Hydrogenases of <i>Ralstonia eutropha</i> H16: Modular Enzymes for Oxygen-Tolerant Biological Hydrogen Oxidation
journal, January 2005

  • Burgdorf, Tanja; Lenz, Oliver; Buhrke, Thorsten
  • Journal of Molecular Microbiology and Biotechnology, Vol. 10, Issue 2-4
  • DOI: 10.1159/000091564

Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats
journal, March 1983


Sodium Ion Cycle in Bacterial Pathogens: Evidence from Cross-Genome Comparisons
journal, September 2001


Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology
journal, November 2012


Na+-translocating NADH: Quinone oxidoreductase: Progress achieved and prospects of investigations
journal, February 2005


Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges
journal, July 2013

  • Kamke, Janine; Sczyrba, Alexander; Ivanova, Natalia
  • The ISME Journal, Vol. 7, Issue 12
  • DOI: 10.1038/ismej.2013.111

Expression of form I and form II Rubisco in chemoautotrophic symbioses: Implications for the interpretation of stable carbon isotope values
journal, December 1995


Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview
journal, October 2007

  • Vignais, Paulette M.; Billoud, Bernard
  • Chemical Reviews, Vol. 107, Issue 10, p. 4206-4272
  • DOI: 10.1021/cr050196r

Ammonium and free amino acids as nitrogen sources for the chemoautotrophic symbiosis Solemya reidi Bernard (Bivalvia : Protobranchia)
journal, June 1992

  • Lee, Raymond W.; Thuesen, Erik V.; Childress, James J.
  • Journal of Experimental Marine Biology and Ecology, Vol. 158, Issue 1
  • DOI: 10.1016/0022-0981(92)90309-x

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Reductive genome evolution in chemoautotrophic intracellular symbionts of deep-sea Calyptogena clams
journal, February 2008


A Second Soluble Hox-Type NiFe Enzyme Completes the Hydrogenase Set in Thiocapsa roseopersicina BBS
journal, June 2010

  • Maroti, J.; Farkas, A.; Nagy, I. K.
  • Applied and Environmental Microbiology, Vol. 76, Issue 15
  • DOI: 10.1128/AEM.00351-10

Hydrogen is an energy source for hydrothermal vent symbioses
journal, August 2011

  • Petersen, Jillian M.; Zielinski, Frank U.; Pape, Thomas
  • Nature, Vol. 476, Issue 7359
  • DOI: 10.1038/nature10325

Reduced Genome of the Thioautotrophic Intracellular Symbiont in a Deep-Sea Clam, Calyptogena okutanii
journal, May 2007


RefSeq microbial genomes database: new representation and annotation strategy
journal, March 2015

  • Tatusova, T.; Ciufo, S.; Fedorov, B.
  • Nucleic Acids Research, Vol. 43, Issue 7
  • DOI: 10.1093/nar/gkv278

Integrative analysis of environmental sequences using MEGAN4
journal, June 2011

  • Huson, D. H.; Mitra, S.; Ruscheweyh, H. -J.
  • Genome Research, Vol. 21, Issue 9
  • DOI: 10.1101/gr.120618.111

Correlations Between Bacterial Ecology and Mobile DNA
journal, June 2010


Physiology, morphology, and biochemical composition of Riftia pachyptila at Rose Garden in 1985
journal, October 1988

  • Fisher, C. R.; Childress, J. J.; Arp, A. J.
  • Deep Sea Research Part A. Oceanographic Research Papers, Vol. 35, Issue 10-11
  • DOI: 10.1016/0198-0149(88)90047-7

Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont
journal, August 2013

  • Nakagawa, Satoshi; Shimamura, Shigeru; Takaki, Yoshihiro
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.131

Status quo in physiological proteomics of the uncultured Riftia pachyptila endosymbiont
journal, June 2011

  • Markert, Stephanie; Gardebrecht, Antje; Felbeck, Horst
  • PROTEOMICS, Vol. 11, Issue 15
  • DOI: 10.1002/pmic.201100059

GuiTope: an application for mapping random-sequence peptides to protein sequences
journal, January 2012

  • Halperin, Rebecca F.; Stafford, Phillip; Emery, Jack S.
  • BMC Bioinformatics, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2105-13-1

A Genomic Perspective on Protein Families
journal, October 1997


Nitrate respiration in the hydrothermal vent tubeworm Riftia pachyptila
journal, December 1993


Metagenome of a Versatile Chemolithoautotroph from Expanding Oceanic Dead Zones
journal, October 2009


Bacterial endosymbioses in Solemya (Mollusca: Bivalvia)—Model systems for studies of symbiont–host adaptation
journal, October 2006


The Calyptogena magnifica Chemoautotrophic Symbiont Genome
journal, February 2007


Possible Roles of Sulfur-Containing Amino Acids in a Chemoautotrophic Bacterium-Mollusc Symbiosis
journal, December 2003

  • Joyner, Joanna L.; Peyer, Suzanne M.; Lee, Raymond W.
  • The Biological Bulletin, Vol. 205, Issue 3
  • DOI: 10.2307/1543296

Prokaryotic sulfur oxidation
journal, June 2005

  • Friedrich, Cornelius G.; Bardischewsky, Frank; Rother, Dagmar
  • Current Opinion in Microbiology, Vol. 8, Issue 3
  • DOI: 10.1016/j.mib.2005.04.005

Identifying bacterial genes and endosymbiont DNA with Glimmer
journal, January 2007


Clustal W and Clustal X version 2.0
journal, September 2007


Real-Time DNA Sequencing from Single Polymerase Molecules
journal, January 2009


Cospeciation of chemoautotrophic bacteria and deep sea clams
journal, August 1998

  • Peek, A. S.; Feldman, R. A.; Lutz, R. A.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 17
  • DOI: 10.1073/pnas.95.17.9962

Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics
journal, October 2011

  • Gardebrecht, Antje; Markert, Stephanie; Sievert, Stefan M.
  • The ISME Journal, Vol. 6, Issue 4
  • DOI: 10.1038/ismej.2011.137

Symbiosis insights through metagenomic analysis of a microbial consortium
journal, September 2006

  • Woyke, Tanja; Teeling, Hanno; Ivanova, Natalia N.
  • Nature, Vol. 443, Issue 7114
  • DOI: 10.1038/nature05192

UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007


RefSeq microbial genomes database: new representation and annotation strategy
journal, December 2013

  • Tatusova, Tatiana; Ciufo, Stacy; Fedorov, Boris
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1274

Locating proteins in the cell using TargetP, SignalP and related tools
journal, April 2007

  • Emanuelsson, Olof; Brunak, Søren; von Heijne, Gunnar
  • Nature Protocols, Vol. 2, Issue 4
  • DOI: 10.1038/nprot.2007.131

Regulation of expression of terminal oxidases in Paracoccus denitrificans : Regulation of expression of terminal oxidases
journal, April 2001


Our microbial selves: what ecology can teach us
journal, July 2011

  • Gonzalez, Antonio; Clemente, Jose C.; Shade, Ashley
  • EMBO reports, Vol. 12, Issue 8
  • DOI: 10.1038/embor.2011.137

Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics
journal, March 2008


Characterization of α-Ketoglutarate-dependent Taurine Dioxygenase from Escherichia coli
journal, September 1997

  • Eichhorn, Eric; van der Ploeg, Jan R.; Kertesz, Michael A.
  • Journal of Biological Chemistry, Vol. 272, Issue 37
  • DOI: 10.1074/jbc.272.37.23031

Vertical Transmission of Chemoautotrophic Symbionts in the Bivalve Solemya velum (Bivalvia: Protobranchia)
journal, April 1996

  • Krueger, D. M.; Gustafson, R. G.; Cavanaugh, C. M.
  • The Biological Bulletin, Vol. 190, Issue 2
  • DOI: 10.2307/1542539

On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves
journal, February 2012

  • Roeselers, Guus; Newton, Irene L. G.
  • Applied Microbiology and Biotechnology, Vol. 94, Issue 1
  • DOI: 10.1007/s00253-011-3819-9

Identification of Substrate Contact Residues Important for the Allosteric Regulation of Phosphofructokinase from Eschericia coli
journal, June 2003

  • Fenton, Aron W.; Paricharttanakul, N. Monique; Reinhart, Gregory D.
  • Biochemistry, Vol. 42, Issue 21
  • DOI: 10.1021/bi034273t

Horizontal endosymbiont transmission in hydrothermal vent tubeworms
journal, May 2006

  • Nussbaumer, Andrea D.; Fisher, Charles R.; Bright, Monika
  • Nature, Vol. 441, Issue 7091
  • DOI: 10.1038/nature04793

Incorporation and utilization of bacterial lipids in theSolemya velum symbiosis
journal, June 1991

  • Conway, N.; McDowell Capuzzo, J.
  • Marine Biology, Vol. 108, Issue 2
  • DOI: 10.1007/bf01344343

Expression of form I and form II Rubisco in chemoautotrophic symbioses: Implications for the interpretation of stable carbon isotope values
journal, December 1995


The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities
journal, December 2010

  • Childress, J. J.; Girguis, P. R.
  • Journal of Experimental Biology, Vol. 214, Issue 2
  • DOI: 10.1242/jeb.049023

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use
journal, April 2012

  • Kleiner, M.; Wentrup, C.; Lott, C.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
  • DOI: 10.1073/pnas.1121198109

Genomics and Evolution of Heritable Bacterial Symbionts
journal, December 2008


Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS
journal, September 2000

  • Shigenobu, Shuji; Watanabe, Hidemi; Hattori, Masahira
  • Nature, Vol. 407, Issue 6800
  • DOI: 10.1038/35024074

Immunochemical localization of ribulose-1,5-bisphosphate carboxylase in the symbiont-containing gills of Solemya velum (Bivalvia: Mollusca)
journal, October 1988

  • Cavanaugh, C. M.; Abbott, M. S.; Veenhuis, M.
  • Proceedings of the National Academy of Sciences, Vol. 85, Issue 20
  • DOI: 10.1073/pnas.85.20.7786

The role of endosymbiotic bacteria in the nutrition of Solemya velum: Evidence from a stable isotope analysis of endosymbionts and host
journal, January 1989

  • Conway, Noellette; Capuzzo, Judith McDowell; Fry, Brian
  • Limnology and Oceanography, Vol. 34, Issue 1
  • DOI: 10.4319/lo.1989.34.1.0249

Insect endosymbionts: manipulators of insect herbivore trophic interactions?
journal, May 2010


WITHDRAWN: An Evaluation of Modern Pottery from Southern Africa as a Magnetic Recorder
journal, December 2012

  • Neukirch, Levi P.; Tarduno, John A.; Cottrell, Rory D.
  • Geochemistry, Geophysics, Geosystems, Vol. 13, Issue 12
  • DOI: 10.1029/2011gc003955

On the origin of mitosing cells
journal, March 1967


The hydrogenases of Thiocapsa roseopersicina
journal, February 2005

  • Kovács, K. L.; Kovács, Á. T.; Maróti, G.
  • Biochemical Society Transactions, Vol. 33, Issue 1
  • DOI: 10.1042/BST0330061

Accelerated evolution and Muller's rachet in endosymbiotic bacteria.
journal, April 1996


OASIS: an automated program for global investigation of bacterial and archaeal insertion sequences
journal, August 2012

  • Robinson, David G.; Lee, Ming-Chun; Marx, Christopher J.
  • Nucleic Acids Research, Vol. 40, Issue 22
  • DOI: 10.1093/nar/gks778

Characterization of the pyrophosphate-dependent 6-phosphofructokinase from Methylococcus capsulatus Bath
journal, November 2008


Lateral Symbiont Acquisition in a Maternally Transmitted Chemosynthetic Clam Endosymbiosis
journal, February 2008

  • Stewart, F. J.; Young, C. R.; Cavanaugh, C. M.
  • Molecular Biology and Evolution, Vol. 25, Issue 4
  • DOI: 10.1093/molbev/msn010

Lateral Phage Transfer in Obligate Intracellular Bacteria (Wolbachia): Verification from Natural Populations
journal, November 2009

  • Chafee, M. E.; Funk, D. J.; Harrison, R. G.
  • Molecular Biology and Evolution, Vol. 27, Issue 3
  • DOI: 10.1093/molbev/msp275

Detection of gene pathways with predictive power for breast cancer prognosis
journal, January 2010


Intense Transpositional Activity of Insertion Sequences in an Ancient Obligate Endosymbiont
journal, June 2008

  • Cordaux, R.; Pichon, S.; Ling, A.
  • Molecular Biology and Evolution, Vol. 25, Issue 9
  • DOI: 10.1093/molbev/msn134

A challenge for 21st century molecular biology and biochemistry: what are the causes of obligate autotrophy and methanotrophy?
journal, June 2004


Phylogenomics of the Reproductive Parasite Wolbachia pipientis wMel: A Streamlined Genome Overrun by Mobile Genetic Elements
journal, March 2004


A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum.
journal, March 1996


Evolutionary microbial genomics: insights into bacterial host adaptation
journal, June 2010

  • Toft, Christina; Andersson, Siv G. E.
  • Nature Reviews Genetics, Vol. 11, Issue 7
  • DOI: 10.1038/nrg2798

One Bacterial Cell, One Complete Genome
journal, April 2010


CO2 Uptake and Fixation by Endosymbiotic Chemoautotrophs from the Bivalve Solemya velum
journal, December 2006

  • Scott, Kathleen M.; Cavanaugh, Colleen M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 4
  • DOI: 10.1128/AEM.01817-06

Suspension feeding on phytoplankton by Solemya velum, a symbiont-containing clam
journal, January 1992

  • Krueger, Dm; Gallager, Sm; Cavanaugh, Cm
  • Marine Ecology Progress Series, Vol. 86
  • DOI: 10.3354/meps086145

Phylogenetic diversity of bacterial symbionts of Solemya hosts based on comparative sequence analysis of 16S rRNA genes
journal, January 1997


Metatranscriptomic Analysis of Sulfur Oxidation Genes in the Endosymbiont of Solemya Velum
journal, January 2011


Sulfur Metabolism in Phototrophic Sulfur Bacteria
book, January 2008


Bacterial Sulfur Globules: Occurrence, Structure and Metabolism
book, January 2006


Structure, function and evolution of bacterial ferredoxins
journal, April 1988


A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum.
journal, March 1996


The bacterial cytochrome cbb3 oxidases
journal, April 2004

  • Pitcher, Robert S.; Watmough, Nicholas J.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1655
  • DOI: 10.1016/j.bbabio.2003.09.017

Gradients in dimethylsulfide, dimethylsulfoniopropionate, dimethylsulfoxide, and bacteria near the sea surface
journal, January 2005

  • Zemmelink, Hj; Houghton, L.; Sievert, Sm
  • Marine Ecology Progress Series, Vol. 295
  • DOI: 10.3354/meps295033

Insights into the Genome of Large Sulfur Bacteria Revealed by Analysis of Single Filaments
journal, August 2007


The path of Carbon in Photosynthesis
journal, August 1950


Assimilation of Inorganic Nitrogen by Marine Invertebrates and Their Chemoautotrophic and Methanotrophic Symbionts
journal, June 1994


Pathways of inorganic nitrogen assimilation in chemoautotrophic bacteria–marine invertebrate symbioses: expression of host and symbiont glutamine synthetase
journal, February 1999

  • Lee, Raymond W.; Robinson, Jonathan J.; Cavanaugh, Colleen M.
  • Journal of Experimental Biology, Vol. 202, Issue 3
  • DOI: 10.1242/jeb.202.3.289

Nitrogen Metabolites and Related Enzymatic Activities in the Body Fluids and Tissues of the Hydrothermal Vent Tubeworm Riftia Pachyptila
journal, October 2000

  • De Cian, Marie-Cécile; Regnault, Michèle; Lallier, François H.
  • Journal of Experimental Biology, Vol. 203, Issue 19
  • DOI: 10.1242/jeb.203.19.2907

Developmental fate of Rhizobium meliloti bacteroids in alfalfa nodules
journal, September 1980


ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria
journal, October 2011

  • Bi, Dexi; Xu, Zhen; Harrison, Ewan M.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr846

ACLAME: A CLAssification of Mobile genetic Elements, update 2010
journal, November 2009

  • Leplae, Raphaël; Lima-Mendez, Gipsi; Toussaint, Ariane
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp938

Works referencing / citing this record:

Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species
journal, December 2018


Horizontal transmission and recombination maintain forever young bacterial symbiont genomes
journal, April 2020

  • Russell, Shelbi L.; Pepper, Evan; Svedberg, Jesper
  • PLOS Genetics
  • DOI: 10.1101/754028

Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses
posted_content, September 2018


Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula
journal, April 2019

  • Jäckle, Oliver; Seah, Brandon K. B.; Tietjen, Målin
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 17
  • DOI: 10.1073/pnas.1818995116

Metagenomic analysis suggests broad metabolic potential in extracellular symbionts of the bivalve Thyasira cf. gouldi
journal, March 2020


The role of microbial motility and chemotaxis in symbiosis
journal, March 2019

  • Raina, Jean-Baptiste; Fernandez, Vicente; Lambert, Bennett
  • Nature Reviews Microbiology, Vol. 17, Issue 5
  • DOI: 10.1038/s41579-019-0182-9

Surfing the vegetal pole in a small population: extracellular vertical transmission of an 'intracellular' deep-sea clam symbiont
journal, May 2016

  • Ikuta, Tetsuro; Igawa, Kanae; Tame, Akihiro
  • Royal Society Open Science, Vol. 3, Issue 5
  • DOI: 10.1098/rsos.160130