Common extracellular sensory domains in transmembrane receptors for diverse signal transduction pathways in bacteria and archaea

Abstract

Transmembrane receptors in microorganisms, such as sensory histidine kinases and methyl-accepting chemotaxis proteins, are molecular devices for monitoring environmental changes. We report here that sensory domain sharing is widespread among different classes of transmembrane receptors. We have identified two novel conserved extracellular sensory domains, named CHASE2 and CHASE3, that are found in at least four classes of transmembrane receptors: histidine kinases, adenylate cyclases, predicted diguanylate cyclases, and either serine/threonine protein kinases (CHASE2) or methyl-accepting chemotaxis proteins (CHASE3). Three other extracellular sensory domains were shared by at least two different classes of transmembrane receptors: histidine kinases and either diguanylate cyclases, adenylate cyclases, or phosphodiesterases. These observations suggest that microorganisms use similar conserved domains to sense similar environmental signals and transmit this information via different signal transduction pathways to different regulatory circuits: transcriptional regulation (histidine kinases), chemotaxis (methyl-accepting proteins), catabolite repression (adenylate cyclases), and modulation of enzyme activity (diguanylate cyclases and phosphodiesterases). The variety of signaling pathways using the CHASE-type domains indicates that these domains sense some critically important extracellular signals.

FIG. 1.

Multiple alignment of CHASE2 domains. The predicted secondary-structure elements are shown above the alignment: cylinders indicate α-helices, and arrows indicate β-strands. Amino acid residues are colored according to an 80% consensus calculated for an extended alignment, which included sequences from unfinished microbial genomes (data not shown): polar (p; KRHEDQNST) in red; bulky hydrophobic (h; ALIVMYFW) and the aliphatic subset of these (l; ILMV) with yellow background; aromatic (a; FHWY) in white with green background; tiny (u; AGS) in white with blue background; small (s; ACDGNPSTV) in blue; and charged (c; DEHKR) and the positively (+; HKR) or negatively (−; DE) subset of these in white with red background. Abbreviations: AC, adenylate cyclase; GGDEF, diguanylate cyclase; HK, histidine kinase; STK, serine/threonine kinase; TIR, the TIR domain-containing protein; UP, unknown protein. Species abbreviations: Ccre, Caulobacter crescentus; Drad, Deinococcus radiodurans; Nos, Nostoc (Anabaena) sp.; Paer, Pseudomonas aeruginosa; Rsol, Ralstonia solanacearum; Smel, Sinorhizobium meliloti; Syn, Synechocystis sp. The last column shows the NCBI protein database gene identification (gi) numbers.

FIG. 2.

Domain architectures of CHASE2-containing proteins. Abbreviations are described in the legend to Fig. 1. Domain architectures are from SMART (39), with modifications.

FIG. 3.

Multiple alignment of the CHASE3 domain. Secondary-structure elements and consensus amino acids are described in the legend to Fig. 1. Species abbreviations: Atum, Agrobacterium tumefaciens; Bhal, Bacillus halodurans; Bsub, Bacillus subtilis; Ccre, Caulobacter crescentus; Drad, Deinococcus radiodurans; Mlot, Mezorhizobium loti; Nos, Nostoc (Anabaena) sp.; Rsol, Ralstonia solanacearum; Scoe, Streptomyces coelicolor; Spla, Spirulina platensis; Vcho, Vibrio cholerae.

FIG. 4.

Domain architectures of CHASE3-containing proteins. Abbreviations are described in the legends to Fig. 1 and 3. Domain architectures are from SMART (39), with modifications.

FIG. 5.

Multiple alignment of CHASE4 domains. Secondary-structure elements and consensus amino acids are described in the legend to Fig. 1. Species abbreviations: Aful, Archaeoglobus fulgidus; Atum, Agrobacterium tumefaciens; Ccre, Caulobacter crescentus; Mace, Methanosarcina acetivorans; Paer, Pseudomonas aeruginosa; Smel, Sinorhizobium meliloti; Sput, Shewanella putrefaciens; Vcho, Vibrio cholerae; Ypes, Yersinia pestis.

FIG. 6.

Domain architectures of CHASE4-containing proteins. Abbreviations are described in the legends to Fig. 1 and 5. Domain architectures are from SMART (39), with modifications.

FIG. 7.

Multiple alignments of CHASE5 (A) and CHASE6 (B) domains. Secondary-structure elements and domain abbreviations are described in the legend to Fig. 1 except for HDc, the phosphohydrolase (phosphodiesterase) domain. Species abbreviations: Atum, Agrobacterium tumefaciens; Hal, Halobacterium sp.; Nos, Nostoc (Anabaena) sp.; Paer, Pseudomonas aeruginosa; Syn, Synechocystis sp.; Vcho, Vibrio cholerae.