Abstract
The uncultivated bacterial endosymbionts of the hydrothermal vent tubeworm Riftia pachyptila play a central role in providing their host with fixed carbon. While this intimate association between host and symbiont indicates tight integration and coordination of function via cellular communication mechanisms, no such systems have been identified. To elucidate potential signal transduction pathways in symbionts that may mediate symbiont-host communication, we cloned and characterized a gene encoding a histidine protein kinase homolog isolated from a symbiont fosmid library. The gene, designated rssA (for Riftia symbiont signal kinase), resembles known sensor kinases and encodes a protein capable of phosphorylating response regulators in Escherichia coli. A second open reading frame, rssB (for Riftia symbiont signal regulator), encodes a protein similar to known response regulators. These results suggest that the symbionts utilize a phosphotransfer signal transduction mechanism to communicate external signals that may mediate recognition of or survival within the host. The specific signals eliciting a response by the signal transduction proteins of the symbiont remain to be elucidated.
MeSH Terms
Amino Acid Sequence
Animals
Bacteria/enzymology,genetics,isolation & purification
Base Sequence
Chromosome Mapping
Cloning, Molecular
DNA Primers/genetics
DNA, Bacterial/genetics
Gene Expression Regulation, Bacterial
Genes, Bacterial
Histidine Kinase
Molecular Sequence Data
Open Reading Frames
Polychaeta/microbiology
Polymerase Chain Reaction
Protein Kinases/genetics
Sequence Homology, Amino Acid
Signal Transduction
Symbiosis
Chemicals
DNA Primers
DNA, Bacterial
Protein Kinases
Histidine Kinase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hughes D S
Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, California 92093-0202, USA.
Felbeck H
Stein J L
References (26)
26 references, click to expand
-
A molecular analysis of the 53.3 minute region of the Escherichia coli linkage map.
J Gen Microbiol. 1991 Feb;137(2):361-7
PMID: 2016588
-
The lemA gene required for pathogenicity of Pseudomonas syringae pv. syringae on bean is a member of a family of two-component regulators.
J Bacteriol. 1992 May;174(9):3011-20
PMID: 1314807
-
Characterization of uncultivated prokaryotes: isolation and analysis of a 40-kilobase-pair genome fragment from a planktonic marine archaeon.
J Bacteriol. 1996 Feb;178(3):591-9
PMID: 8550487
-
Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris.
Mol Gen Genet. 1991 May;226(3):409-17
PMID: 1645442
-
Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.
Science. 1993 Oct 22;262(5133):539-44
PMID: 8211181
-
Response regulators of bacterial signal transduction systems: selective domain shuffling during evolution.
J Mol Evol. 1995 Feb;40(2):136-54
PMID: 7699720
-
Sensor and regulator proteins from the cyanobacterium Synechococcus species PCC7942 that belong to the bacterial signal-transduction protein families: implication in the adaptive response to phosphate limitation.
Mol Microbiol. 1993 Apr;8(1):81-91
PMID: 8497200
-
Eukaryotes have "two-component" signal transducers.
Res Microbiol. 1994 Jun-Aug;145(5-6):481-6
PMID: 7855435
-
Whole-genome random sequencing and assembly of Haemophilus influenzae Rd.
Science. 1995 Jul 28;269(5223):496-512
PMID: 7542800
-
Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins.
Proc Natl Acad Sci U S A. 1989 Sep;86(17):6671-5
PMID: 2549542
-
Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. I. Sequence features in the 1 Mb region from map positions 64% to 92% of the genome.
DNA Res. 1995 Aug 31;2(4):153-66, 191-8
PMID: 8590279
-
Communication modules in bacterial signaling proteins.
Annu Rev Genet. 1992;26:71-112
PMID: 1482126
-
A novel sensor-regulator protein that belongs to the homologous family of signal-transduction proteins involved in adaptive responses in Escherichia coli.
Mol Microbiol. 1992 Mar;6(6):799-807
PMID: 1574005
-
Sulfur-oxidizing bacterial endosymbionts: analysis of phylogeny and specificity by 16S rRNA sequences.
J Bacteriol. 1988 Jun;170(6):2506-10
PMID: 3286609
-
An Agrobacterium two-component regulatory system for the detection of chemicals released from plant wounds.
Mol Microbiol. 1991 Oct;5(10):2345-50
PMID: 1791750
-
Systematic sequencing of the 180 kilobase region of the Bacillus subtilis chromosome containing the replication origin.
DNA Res. 1994;1(1):1-14
PMID: 7584024
-
A yeast protein similar to bacterial two-component regulators.
Science. 1993 Oct 22;262(5133):566-9
PMID: 8211183
-
RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli.
J Bacteriol. 1990 Feb;172(2):659-69
PMID: 2404948
-
Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis.
Nature. 1989 Feb 23;337(6209):745-9
PMID: 2645526
-
Identification and localization of bacterial endosymbionts in hydrothermal vent taxa with symbiont-specific polymerase chain reaction amplification and in situ hybridization techniques.
Mol Mar Biol Biotechnol. 1993 Feb;2(1):51-62
PMID: 8364689
-
Riftia pachyptila Jones: Observations on the Vestimentiferan Worm from the Galapagos Rift.
Science. 1981 Jul 17;213(4505):333-6
PMID: 17819904
-
Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions.
DNA Res. 1996 Jun 30;3(3):109-36
PMID: 8905231
-
Protein phosphorylation and regulation of adaptive responses in bacteria.
Microbiol Rev. 1989 Dec;53(4):450-90
PMID: 2556636
-
Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus.
Mol Microbiol. 1994 Jan;11(1):137-53
PMID: 7908398
-
Deduced product of the stage 0 sporulation gene spo0F shares homology with the Spo0A, OmpR, and SfrA proteins.
Proc Natl Acad Sci U S A. 1985 Nov;82(21):7260-4
PMID: 2997779
-
A two-component system that regulates an osmosensing MAP kinase cascade in yeast.
Nature. 1994 May 19;369(6477):242-5
PMID: 8183345