Interplay of heritage and habitat in the distribution of bacterial signal transduction systems

Abstract

Comparative analysis of the complete genome sequences from a variety of poorly studied organisms aims at predicting ecological and behavioral properties of these organisms and helping in characterizing their habitats. This task requires finding appropriate descriptors that could be correlated with the core traits of each system and would allow meaningful comparisons. Using the relatively simple bacterial models, first attempts have been made to introduce suitable metrics to describe the complexity of organism's signaling machinery, which included introducing the "bacterial IQ" score. Here, we use an updated census of prokaryotic signal transduction systems to improve this parameter and evaluate its consistency within selected bacterial phyla. We also introduce a more elaborate descriptor, a set of profiles of relative abundance of members of each family of signal transduction proteins encoded in each genome. We show that these family profiles are well conserved within each genus and are often consistent within families of bacteria. Thus, they reflect evolutionary relationships between organisms as well as individual adaptations of each organism to its specific ecological niche.

Figure 1. Relationship between the number of signal transduction proteins and the total number of proteins encoded in that genome

The phylogenetic affiliation of the source genomes is indicated as follows: Actinobacteria, yellow circles; Cyanobacteria, cyan circles; Proteobacteria, empty squares; Firmicutes, blue triangles; members of the CFB group (phyla Bacteroidetes and Chlorobi), green triangles; members of other bacterial phyla, pink triangles. Archaeal genomes are not shown but have been included in the calculation of the best fit.

Figure 2. Signal transduction protein family profiles for 10 mycobacterial genomes

The source organisms are indicated by the following colors: Mycobacterium leprae TN, purple; M. bovis AF2122/97, pink; M. tuberculosis H37Rv, red; M. ulcerans Agy99, buff; M. avium subsp. paratuberculosis K-10, blue; M. abscessus, salmon; M. marinum M, green; M. gilvum PYR-GCK, lavender; M. vanbaalenii PYR-1, pale lavender; M. smegmatis str. MC2 155, light blue.

Figure 3. Signal transduction protein family profiles for Shewanella species

The source organisms are shown in the following order: Shewanella denitrificans OS217, Shewanella halifaxensis HAW-EB4, Shewanella pealeana ATCC 700345, Shewanella frigidimarina NCIMB 4, Shewanella putrefaciens CN-32, Shewanella piezotolerans WP3, Shewanella loihica PV-4, Shewanella amazonensis SB2B, Shewanella oneidensis MR-1, Shewanella baltica OS155, Shewanella woodyi ATCC 51908, Shewanella sediminis HAW-EB3.

Figure 4. Signal transduction protein family profiles for various bacilli

Family profiles of the representatives of family Bacillaceae (A), order Bacillales (B), class Bacilli (C) and the phylum Firmicutes (D). A. The source organisms are shown in the following order: Oceanobacillus iheyensis HTE831, Anoxybacillus flavithermus WK1, Geobacillus kaustophilus HTA426, Geobacillus thermodenitrificans NG80-2, Bacillus pumilus SAFR-032, B. subtilis subsp. subtilis str. 168, B. amyloliquefaciens FZB42, B. licheniformis ATCC 14580, B. clausii KSM-K16, B. halodurans C-125, B. anthracis str. Ames, B. cereus ATCC 14579, B. thuringiensis serovar konkukian str. 97-27, B. weihenstephanensis KBAB4. B. The source organisms are as in panel A, with the addition of Staphylococcus epidermidis ATCC 12228, Staph. haemolyticus JCSC1435, Staph. aureus subsp. aureus N315, Listeria monocytogenes EGD-e, Listeria innocua Clip11262, and Lysinibacillus sphaericus C3-41. C. The source organisms are as in panel B, with the addition of Lactobacillus helveticus DPC 4571, Lactococcus lactis subsp. lactis Il1403, Streptococcus pyogenes M1 GAS, Strep. mutans UA159, and Strep. pneumoniae TIGR4. D. A heat map of signal transduction protein family profiles of 78 Firmicute species, clustered by the number of proteins of different types normalized by the proteome size. For each organism, the number of signal transduction proteins was divided by the square of the total number of encoded proteins (a log of this value is roughly equivalent to the IQ score) and then transformed to ranks to remove the influence of outliers and asymmetry in the distributions. The neighbor-joining tree of these ranks clearly separates members of the Bacilli (upper half) and the Clostridia (bottom half). The organisms with low IQs (shades of blue) tend to cluster toward the top of heat map while the higher IQs (shades of red) cluster toward the bottom.