Evolution of the PPM-family protein phosphatases in Streptomyces: duplication of catalytic domain and lateral recruitment of additional sensory domains

Abstract

Originally identified from eukaryotes, the Mg 2+ -or Mn 2+ -dependent protein phosphatases (PPMs) are a diverse group of enzymes whose members include eukaryotic PP2C and some prokaryotic serine/threonine phosphatases. In a previous study, unexpectedly large numbers of PPMs were identified in two Streptomyces genomes. In this work, a phylogenetic analysis was performed with all the PPMs available from a wide variety of microbial sources to determine the evolutionary origin of the Streptomyces PPM proteins. Consistent with earlier hypotheses, the results suggested that the microbial PPMs were relatively recent additions from eukaryotic sources. Results also indicated that the Streptomyces PPMs were divided into two major subfamilies at an early stage of their emergence in Streptomyces genomes. The first subfamily, which contains only six Streptomyces PPMs, possesses a catalytic domain whose sequence and architecture are similar to that of eukaryotic PPMs; the second subfamily contains 89 Streptomyces PPMs that lack the 5a and 5b catalytic domain motifs, similar to the PPMs SpoIIE and RsbU of Bacillus subtilis. Significant gene duplication was observed for the PPMs in the second subfamily. In addition, more than half (54 %) of the Streptomyces PPMs from the second subfamily were found to have at least one additional sensory domain, most commonly the PAS or the GAF domain. Phylogenetic analysis showed that these domains tended to be clustered according to the putative physiological functions rather than taxonomic relationship, implying that they might have arisen as a result of domain recruitment in a late evolutionary stage. This study provides an insight into how Streptomyces spp. may have expanded their PPM-based signal transduction networks to enable them to respond to a greater range of environmental changes.

Eukaryote-Like Serine/Threonine Kinases and Phosphatases in Bacteria

“…The serine/threonine Mg 2ϩ -or Mn 2ϩ -dependent phosphatases of the PPM family share a conserved catalytic domain with eukaryotic PP2C that contains 11 to 13 signature motifs containing eight conserved amino acids (2,19,78,165,199) (Fig. 6A).…”

“…6A). Bacterial PPMs can be divided into two subfamilies depending on the presence of motifs 5a and 5b (199). One subfamily, which includes the B. subtilis sporulation-specific phosphatase SpoIIE (40) and the stress response phosphatases RsbU and RsbX (34,42,76,126,193), lacks the 5a and 5b catalytic domain motifs (77,199).…”

Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases

“…These sequences were then used in the construction of a phylogenetic tree. To help in the classification and definition of each phylogenetic cluster, a few dozen PAS domains with known function, obtained from other bacterial sources, were also used in the phylogenetic tree construction as described previously Zhang & Shi, 2004). It is obvious from the phylogenetic analysis that, although individual exceptions are present and overall bootstrap support was not high, PAS domains extracted from hybrid-type HKs tend to be clustered based on their putative physiological function rather than taxonomic relationship (data not shown).…”

Identification of Sensory and Signal‐Transducing Domains in Two‐Component Signaling Systems

“…Thus, activities of cyanobacterial membrane-bound adenylate cyclase and Rhodobacter sphaeroides bacteriophytochrome BphG1 (diguanylate cyclase/phosphodiesterase) were shown to respond to the red and blue light (Ohmori and Okamoto, 2004;Tarutina et al, 2006). Activities of many other bacterial receptor-type proteins appear to be regulated by environmental factors as well; however, the nature of these factors still remains obscure (Galperin, 2004(Galperin, , 2005Kennelly, 2002;Lory et al, 2004;Römling et al, 2005;Zhang and Shi, 2004). Still, recognition of a potential receptor protein in a given piece of DNA sequence could be an important step towards understanding the function of that protein and/or its neighbors.…”