Hindawi Publishing Corporation International Journal of Evolutionary Biology Volume 2012, Article ID 745931, 6 pages doi:10.1155/2012/745931 Research Article Evolution of Lysine Biosynthesis in the Phylum Deinococcus-Thermus Hiromi Nishida1 and Makoto Nishiyama2 1 Agricultural Bioinformatics Research Unit, Graduate School of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan 2 Biotechnology Research Center, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan Correspondence should be addressed to Hiromi Nishida, [email protected] Received 28 January 2012; Accepted 17 February 2012 Academic Editor: Kenro Oshima Copyright © 2012 H. Nishida and M. Nishiyama. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Thermus thermophilus biosynthesizes lysine through the α-aminoadipate (AAA) pathway: this observation was the first discovery of lysine biosynthesis through the AAA pathway in archaea and bacteria. Genes homologous to the T. thermophilus lysine biosynthetic genes are widely distributed in bacteria of the Deinococcus-Thermus phylum. Our phylogenetic analyses strongly suggest that a common ancestor of the Deinococcus-Thermus phylum had the ancestral genes for bacterial lysine biosynthesis through the AAA pathway. In addition, our findings suggest that the ancestor lacked genes for lysine biosynthesis through the diaminopimelate (DAP) pathway. Interestingly, Deinococcus proteolyticus does not have the genes for lysine biosynthesis through the AAA pathway but does have the genes for lysine biosynthesis through the DAP pathway. Phylogenetic analyses of D. proteolyticus lysine biosynthetic genes showed that the key gene cluster for the DAP pathway was transferred horizontally from a phylogenetically distant organism. 1. Introduction species acquired genes from various other bacteria to survive different kinds of environmental stresses, whereas Thermus The Deinococcus-Thermus phylum constitutes one of the species have acquired genes from thermophilic bacteria to major bacterial evolutionary lineages [1, 2]. At present, the adapt to high-temperature environments [11]. genome sequence data of 6 genera (13 organisms) belonging The distribution of lysine biosynthetic genes in the to this phylum are available in the Kyoto Encyclopedia of Deinococcus-Thermus phylum has not been clearly described. Genes and Genomes (KEGG) database [3]. In this study, we compared the distribution of the genes Two pathways for lysine biosynthesis have been de- for lysine biosynthesis between 13 organisms (D. deserti, α scribed, namely, the -aminoadipate (AAA) pathway and the D. geothermalis, D. maricopensis, D. proteolyticus, D. radio- diaminopimelate (DAP) pathway [5]. The AAA pathway has durans, Marinithermus hydrothermalis, Meiothermus ruber, ff two di erent types [6]. In T. thermophilus,ageneclusterwas M. silvanus, Oceanithermus profundus, T. scotoductus, T. found for lysine biosynthesis not through the DAP pathway thermophilus HB8, T. thermophilus HB27, and Truepera but through the AAA pathway [6–8]. Although Deinococcus radiovictrix). radiodurans has genes homologous to the T. thermophilus lysine biosynthetic genes, these genes are scattered on the 2. Methods genome [9]. In addition, the D. radiodurans aspartate kinase that catalyzes the phosphorylation of l-aspartate (the first We analyzed the distribution of each of the following reaction in the DAP pathway) is structurally and phylogenet- 10 enzymes related to lysine biosynthesis through the ically very different from that of T. thermophilus [10]. Recent AAA pathway in the Deinococcus-Thermus phylum: α- studies have shown that the genome signatures of these 2 bac- aminoadipate aminotransferase, homoisocitrate dehydro- teria are different [4], supporting the theory that Deinococcus genase, LysW-γ-l-lysine aminotransferase, LysW-γ-l-lysine 2 International Journal of Evolutionary Biology Table 1: Genes for lysine biosynthesis through the α-aminoadipate pathway in the Deinococcus-Thermus phylum. Organism Enzyme 1 Enzyme 2 Enzyme 3 Enzyme 4 Enzyme 5 Enzyme 6 Enzyme 7 Enzyme 8 Enzyme 9 Enzyme 10 Thermus thermophilus HB27 TTC0043 TTC1012 TTC1393 TTC1396 TTC1541∗ TTC1542∗ TTC1543∗ TTC1546∗ TTC1547∗ TTC1550∗ Thermus thermophilus HB8 TTHA0411 TTHA1378 TTHA1755 TTHA1757 TTHA1903∗ TTHA1904∗ TTHA1907∗ TTHA1910∗ TTHA1911∗ TTHA1914∗ Thermus scotoductus TSC c05810 TSC c20650 TSC c03550 TSC c3520 TSC c01940∗ TSC c01930∗ TSC c01920∗ TSC c01890∗ TSC c01880∗ TSC c01850∗ Meiothermus ruber Mrub 0871 Mrub 2738 Mrub 0027 Mrub 2721∗ Mrub 2723∗ Mrub 2724∗ Mrub 2727∗ Mrub 2728∗ Meiothermus silvanus Mesil 2567 Mesil 1337 Mesil 0348 Mesil 0347 Mesil 0435∗ Mesil 0436∗ Mesil 0438∗ Mesil 0441∗ Mesil 0442∗ Oceanithermus profundus Ocepr 1387 Ocepr 1797∗ Ocepr 1798∗ Ocepr 1796∗ Ocepr 1788∗ Ocepr 1784∗ Ocepr 1781∗ Ocepr 1780∗ Ocepr 1779∗ Marinithermus Marky 1533 Marky 0665∗ Marky 0663∗ Marky 0666∗ Marky 0667∗ Marky 0668∗ Marky 0671∗ Marky 0672∗ Marky 0673∗ hydrothermalis Deinococcus radiodurans DR 1674 DR 0794 DR 1413 DR 1420 DR 0963 DR 2194 DR 1614 DR 1610 DR 1238 Deinococcus geothermalis Dgeo 2084 Dgeo 1458 Dgeo 1416 Dgeo 1391 Dgeo 0678 Dgeo 0685 Dgeo 1151∗ Dgeo 1154∗ Dgeo 1156∗ Dgeo 1257 Deinococcus deserti Deide 09240 Deide 16910 Deide 17960 Deide 10430 Deide 10350 Deide 13430∗ Deide 13460∗ Deide 13470∗ Deide 13980 Deinococcus maricopensis Deima 0046 Deima 1545 Deima 2454 Deima 2593 Deima 1346∗ Deima 1349∗ Deima 1350∗ Deima 1353∗ Deima 1355∗ Deima 1358∗ Deinococcus proteolyticus Deipr 0213 Truepera radiovictrix Trad 2841 Trad 1401∗ Trad 1404∗ Trad 1399∗ Trad 1395∗ Trad 1392∗ Trad 1390∗ Trad 1389∗ Trad 1388∗ Enzyme 1, α-aminoadipate aminotransferase. Enzyme 2, Homoisocitrate dehydrogenase. Enzyme 3, LysW-γ-l-lysine aminotransferase. Enzyme 4, LysW-γ-l-lysine hydrolase. Enzyme 5, LysW-γ-l-α-aminoadipate kinase. Enzyme 6, LysW-γ-l-α-aminoadipyl-6-phosphate reductase. Enzyme 7, α-aminoadipate-LysW ligase LysX. Enzyme 8, LysU. Enzyme 9, LysT. Enzyme 10, Homocitrate synthase. ∗More than 3 genes are clustered. International Journal of Evolutionary Biology 3 Table 2: Genes for lysine biosynthesis through the diaminopimelate pathway in the Deinococcus-Thermus phylum. Aspartate- ll- Aspartate Dihydrodipicolinate Dihydrodipicolinate Diaminopimelate Organism semialdehyde diaminopimelate kinase synthase reductase decarboxylase dehydrogenase aminotransferase Thermus thermophilus HB27 TTC0166 TTC0177 TTC0591 Thermus thermophilus HB8 TTHA0534 TTHA0545 TTHA0957 Thermus scotoductus TSC c07050 TSC c08140 TSC c10420 TSC c10870 Meiothermus ruber Mrub 0976 Mrub 1641 Mrub 1335 Mrub 0798 Meiothermus silvanus Mesil 1711 Mesil 2173 Mesil 2308 Mesil 0318 Oceanithermus profundus Ocepr 1316 Ocepr 1018 Ocepr 2076 Marinithermus Marky 1492 Marky 1381 Marky 1261 hydrothermalis Deinococcus radiodurans DR 1365 DR 2008 DR 1758 Deinococcus geothermalis Dgeo 1127 Dgeo 1782 Dgeo 0790 Deide 1p00310, Deide 12830, Deinococcus deserti Deide 11430 Deide 15740 Deide 3p00120, Deide 21880 Deide 3p01100 Deinococcus maricopensis Deima 1822 Deima 2680 Deima 2660 Deipr 0627, Deinococcus proteolyticus Deipr 0941 Deipr 0985 Deipr 1377∗ Deipr 1378∗ Deipr 1376∗ Deipr 1375∗ Truepera radiovictrix Trad 0977 Trad 0289 Trad 1893 Trad 0134 ∗ More than 3 genes are clustered. 33 Spirochaeta thermophila STHERM c00170 16 Denitrovibrio acetiphilus Dacet 0798 Spirochaeta caldaria DSM 7334 Spica 0951 35 100 Treponema primitia TREPR 1186 Calditerrivibrio nitroreducens Calni 0514 35 89 Flexistipes sinusarabici Flexsi 1574 97 Methanohalophilus mahii Mmah 0892 Methanococcoides burtonii Mbur 0628 98 100 Methanosarcina barkeri Mbar A1641 100 Methanosarcina mazei MM 1885 100 Methanosarcina acetivorans MA0726 Selenomonas sputigena Selsp 2045 56 Syntrophobotulus glycolicus Sgly 1852 61 Desulfitobacterium hafniense DCB-2 Dhaf 4876 100 Desulfitobacterium hafniense Y51 DSY4977 Spirochaeta smaragdinae Spirs 1460 100 Deinococcus proteolyticus Deipr 1375 Kytococcus sedentarius Ksed 00760 100 Spirochaeta sp. Buddy SpiBuddy 1124 100 Spirochaeta coccoides Spico 0777 0.1 Figure 1: Phylogenetic relationship between Deinococcus proteolyticus diaminopimelate decarboxylase and related proteins. Multiple alignment was obtained using the top 20 amino acid sequences of the BLASTp search result for D. proteolyticus diaminopimelate decarboxylase (Deipro 1375), as based on the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. The maximum-likelihood tree was constructed using MEGA software version 5 [12]. The WAG model was used as the amino acid substitution model. The nearest neighbor interchange was used for the maximum-likelihood heuristic method. The γ-distributed rate was considered, and the number of discrete γ categories was 3. Bootstrap analysis was performed with 100 replicates. Red indicates D. proteolyticus. 4 International Journal of Evolutionary Biology 100 Anabaena variabilis Ava 2354 59 Anabaena sp. PCC7120 alr5103 81 Cyanothece sp. PCC 7425 Cyan7425 4424 89 Acaryochloris marina AM1 1880 87 Synechococcus elongatus PCC7942 Synpcc7942 0853 100 Synechococcus elongatus PCC6301 syc0687 c 72 Synechococcus sp. CC9605 Syncc9605 0311 Opitutus terrae Oter 4620 Pelobacter carbinolicus Pcar 2423 100 Geobacter sp. M21 GM21 4142 100 Geobacter bemidjiensis Gbem 4052 94 Geobacter metallireducens Gmet 0213 100 Geobacter uraniumreducens Gura 0238 74 Geobacter sp. FRC-32 Geob 1134 50 Geobacter lovleyi Glov 3040 Spirochaeta