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Proteobacterial Genomes

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Proteobacterial Genomes Distinguishing features of ␦-proteobacterial genomes Samuel Karlin*†, Luciano Brocchieri*, Jan Mra´ zek‡, and Dale Kaiser§ Departments of *Mathematics and §Biochemistry, Stanford University, Stanford, CA 94305; and ‡Department of Microbiology, University of Georgia, Athens, GA 30602 Contributed by Samuel Karlin, June 5, 2006 We analyzed several features of five currently available ␦- Table 1. ␦-Proteobacterial complete genomes proteobacterial genomes, including two aerobic bacteria exhibit- G ϩ C genome ing predatory behavior and three anaerobic sulfate-reducing bac- frequencies, % % PHX genes, % Max E(g) teria. The ␦ genomes are distinguished from other bacteria by several properties: (i) The ␦ genomes contain two ‘‘giant’’ S1 MYXXA 68.9 19.2 2.02 ribosomal protein genes in contrast to all other bacterial types, BDEBA 50.7 7.3 2.87 which encode a single or no S1; (ii) in most ␦-proteobacterial DESVU 63.2 15.1 1.90 GEOSU 60.9 5.2 1.33 genomes the major ribosomal protein (RP) gene cluster is near the DESPS 46.8 8.6 1.63 replication terminus whereas most bacterial genomes place the major RP cluster near the origin of replication; (iii) the ␦ genomes possess the rare combination of discriminating asparaginyl and glutaminyl tRNA synthetase (AARS) together with the amido- zation of prey bacteria by BDEBA is reviewed in refs 2 and 11. transferase complex (Gat CAB) genes that modify Asp-tRNAAsn into DESVU is a strictly anaerobic sulfate-reducing bacterium (3) with Asn-tRNAAsn and Glu-tRNAGln into Gln-tRNAGln;(iv) the TonB re- a substantial capacity to oxidize metal ions, many of which are toxic. ceptors and ferric siderophore receptors that facilitate uptake and It has an extensive network of periplasmic hydrogenases and removal of complex metals are common among ␦ genomes; (v) the cytochromes for electron transport (3). GEOSU implements biore- anaerobic ␦ genomes encode multiple copies of the anaerobic mediation by precipitating various soluble heavy metals (4). detoxification protein rubrerythrin that can neutralize hydrogen GEOSU encodes many predicted highly expressed (PHX) cyto- peroxide; and (vi) ␴54 activators play a more important role in the chrome c and ferredoxin proteins that are used for periplasmic and ␦ genomes than in other bacteria. ␦ genomes have a plethora of outer membrane electron transport (4). DESPS is a psychrophilic enhancer binding proteins that respond to environmental and sulfate-reducing bacterium that uses sulfate as the main electron intracellular cues, often as part of two-component systems; (vii) ␦ acceptor and lactate and alcohols as major carbon and electron genomes encode multiple copies of metallo-␤-lactamase enzymes; sources (5). Its optimal doubling time is 27 h during growth on (viii) a host of secretion proteins emphasizing SecA, SecB, and SecY lactate at 10°C, but it can also grow successfully at a temperature may be especially useful in the predatory activities of Myxococcus Ͻ0°C (5). xanthus;(ix) ␦ proteobacteria drive many multiprotein machines in This article has two objectives. First, PHX genes and related their periplasms and outer membrane, including chaperone-feed- properties of the five ␦ genomes are analyzed (Table 1). Qualita- ing machines, jets for slime secretion, and type IV pili. Bdellovibrio tively, a gene can be defined PHX if its codon frequencies are replicates in the periplasm of prey cells. The sulfate-reducing ␦ similar to highly expressed genes such as those for ribosomal proteobacteria metabolize hydrogen and generate a proton gra- proteins (RP) or for major transcription͞translation factors (TF) or dient by electron transport. The predicted highly expressed genes for the principal chaperone͞degradation (CH) proteins, but deviate from ␦ genomes reflect their different ecologies, metabolic strat- strongly in codon frequencies from the average gene of the genome egies, and adaptations. (see Methods for precise criteria). Second, various properties that distinguish the ␦ genomes from other bacteria are described. ␦ proteobacteria ͉ Myxococcus xanthus ͉ sulfate-reducing bacteria ͉ predatory bacteria ͉ ␴54 activators Results and Discussion Distinctive PHX Genes of ␦ Genomes. MYXXA shows, to date, the he ␦ proteobacteria (␦ genomes) are defined by their 16S RNA highest percentage of PHX genes, 19.2% compared with all sequence (1). Completely sequenced ␦ genomes include the currently sequenced bacterial genomes (12–16). The top PHX T gene in MYXXA encodes the preprotein SecA translocase multicellular predator Myxococcus xanthus (MYXXA) (D.K., W. C. ϭ Nierman, B. S. Goldman, S. Slater, A. S. Durkini, J. Eisen, C. M. subunit [E(g) 2.02] (see Table 6, which is published as Ronning, W. B. Barbazuk, M. Blanchard, C. Field, et al., unpub- supporting information on the PNAS web site). The high E(g) lished results), the unicellular predator Bdellovibrio bacteriovorus value suggests that secretion plays a major role in the MYXXA lifestyle. Of almost equal predicted expression level are the RNA (BDEBA) (2), and the three anaerobic sulfate-reducing bacteria ϭ ϭ Desulfovibrio vulgaris (DESVU) (3), Geobacter sulfurreducens polymerase subunits RpoC [E(g) 2.02] and RpoB [E(g) 1.84] and the ATP-dependent protease Lon [E(g) ϭ 1.95]. A highly (GEOSU) (4) and Desulfotalea psychrophila (DESPS) (5). Whereas ϭ MYXXA of 9.14-Mb length is among the largest bacterial genomes expressed protein [E(g) 2.01] of unknown function that could sequenced, the other four ␦ genomes are all of size 3.5 to 4.0 Mb. be an attractive candidate for experimental analyses is encoded MYXXA lives in cultivated topsoil, where it is often exposed to at genome positions 4160152–4162320. The PHX genes of solar radiation and is well aerated. It has two life stages, growth and development, both of which involve remarkable cellular coopera- Conflict of interest statement: No conflicts declared. tion and much gliding movement (6–8). Myxobacteria are profi- Abbreviations: PHX, predicted highly expressed; RP, ribosomal protein; AARS, asparaginyl cient predators of whole colonies of other soil microbes. MYXXA and glutaminyl tRNA synthetase; RR, response regulator; HK, histidine kinase; TCA, tricar- encodes many duplicated proteins expressed during the different boxylic acid. life stages, e.g., Lon (9) and serine-threonine protein kinases (10). Data deposition: The two new complete genomes referred to in Note have been deposited BDEBA is ubiquitous in terrestrial and aquatic habitats. It preys on in the GenBank database [accession nos. NC-007519 (Desulfovibrio desulfuricans) and individual Gram-negative bacterial cells by invading their periplasm NC-007517 (Geobacter metallireduceans)]. and transforming them into nearly spherical structures called †To whom correspondence should be addressed. E-mail: [email protected]. bdelloplasts (2). A detailed scenario for the adhesion and coloni- © 2006 by The National Academy of Sciences of the USA 11352–11357 ͉ PNAS ͉ July 25, 2006 ͉ vol. 103 ͉ no. 30 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0604311103 Downloaded by guest on October 2, 2021 Table 2. PHX genes of important pathways Genomes Glycolysis* TCA-cycle* Detoxification* MYXXA 8 (8) 11 (13) 10 (14) BDEBA 3 (3) 7 (8) 5 (5) DESVU 4 (4) 1 (1) 1 (1) Scheme 1. Cluster of six TCA cycle genes. GEOSU 1 (1) 5 (5) 3 (3) DESPS 1 (1) 1 (1) 0 (0) form a gene cluster, possibly a single operon (display in Scheme 1). DESVU has three anaerobic detoxification genes (rubrerythrin, rubredoxin- oxygen oxidoreductase, and nigerythrin). Overall, MYXXA has 11 PHX TCA cycle genes and 13 including *Number of distinct PHX genes (number of PHX genes with repeats). two duplications (Table 2 and Scheme 1). The successive gaps between genes in Scheme 1 are 32, 219, 44, 286, and 29 bp. The successive genes are of sizes 431, 313, 625, 268, 385, and 298 aa. BDEBA reach the high E(g) level 2.87, suggesting that BDEBA Gene orientation is indicated by arrows. The coordinates below the should be considered a fast growing organism (16, 17). In fact, grid indicate the starting position of each gene. once inside the bdelloplast, BDEBA does multiply rapidly, TCA cycle genes of the ␦ genomes BDEBA, GEOSU, and producing several descendants from a single Escherichia coli host DESPS are organized similarly in that sucA is adjacent to sucB, sucC cell (11). BDEBA also encodes a variety of periplasmic PHX is adjacent to sucD, and the succinate dehydrogenase flavoprotein electron transporters that adapt it to microaerophilic conditions subunit (sdhA) and the succinate dehydrogenase iron-sulfur subunit likely found within the host’s periplasm (11). Of the 46 RP genes (sdhB) are encoded as part of a single operon. BDEBA and DESPS Ն80 aa length of the BDEBA genome, 45 are PHX, a high encode complete sets of TCA cycle enzymes (8 and 1, respectively, proportion consistent with the proposition that BDEBA is fast PHX). DESVU features a fusion of sucC and sucD (sucCD) but, growing (17). DESVU contains several PHX anaerobic detox- apart from icd (PHX), mdh, and fumC, lacks the other genes of the ification genes, including two rubrerythrin genes and two rubre- TCA cycle. Five TCA cycle enzymes are PHX in GEOSU. doxin oxidoreductase genes that can protect the organism against oxidative stress or other reactive toxins (18, 19). The gene Glycolysis. Genes encoding glycolytic enzymes are broadly distrib- of highest PHX level [E(g) ϭ 1.90] is the large ribosomal protein uted among the ␦ genomes, with a single cluster in each genome. gene S1. The PHX genes of GEOSU encompass only 5% of the Explicitly, MYXXA, BDEBA, and GEOSU each cluster the genes proteome and have a maximum E(g) ϭ 1.33 for the RNA gap, pgk, and tpi, probably in a single operon; DESVU clusters the processing͞degradation gene pnp (polynucleotide phosphory- genes fba and gap; and DESPS clusters tpi and pgk. MYXXA lase). The low expression levels of its PHX genes suggest that contains two copies of pyk and of pfk and DESVU contains two GEOSU is prone to grow slowly (16, 17).
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