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Hindawi Publishing CorporationInternational Journal of Evolutionary BiologyVolume 2012, Article ID 745931, 6 pagesdoi:10.1155/2012/745931

Research Article

Evolution of Lysine Biosynthesis in the PhylumDeinococcus-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 CommonsAttribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work isproperly cited.

Thermus thermophilus biosynthesizes lysine through the α-aminoadipate (AAA) pathway: this observation was the first discoveryof lysine biosynthesis through the AAA pathway in archaea and bacteria. Genes homologous to the T. thermophilus lysinebiosynthetic genes are widely distributed in bacteria of the Deinococcus-Thermus phylum. Our phylogenetic analyses stronglysuggest that a common ancestor of the Deinococcus-Thermus phylum had the ancestral genes for bacterial lysine biosynthesisthrough the AAA pathway. In addition, our findings suggest that the ancestor lacked genes for lysine biosynthesis through thediaminopimelate (DAP) pathway. Interestingly, Deinococcus proteolyticus does not have the genes for lysine biosynthesis throughthe AAA pathway but does have the genes for lysine biosynthesis through the DAP pathway. Phylogenetic analyses of D. proteolyticuslysine biosynthetic genes showed that the key gene cluster for the DAP pathway was transferred horizontally from a phylogeneticallydistant organism.

1. Introduction

The Deinococcus-Thermus phylum constitutes one of themajor bacterial evolutionary lineages [1, 2]. At present, thegenome sequence data of 6 genera (13 organisms) belongingto this phylum are available in the Kyoto Encyclopedia ofGenes and Genomes (KEGG) database [3].

Two pathways for lysine biosynthesis have been de-scribed, namely, the α-aminoadipate (AAA) pathway and thediaminopimelate (DAP) pathway [5]. The AAA pathway hastwo different types [6]. In T. thermophilus, a gene cluster wasfound for lysine biosynthesis not through the DAP pathwaybut through the AAA pathway [6–8]. Although Deinococcusradiodurans has genes homologous to the T. thermophiluslysine biosynthetic genes, these genes are scattered on thegenome [9]. In addition, the D. radiodurans aspartate kinasethat catalyzes the phosphorylation of l-aspartate (the firstreaction in the DAP pathway) is structurally and phylogenet-ically very different from that of T. thermophilus [10]. Recentstudies have shown that the genome signatures of these 2 bac-teria are different [4], supporting the theory that Deinococcus

species acquired genes from various other bacteria to survivedifferent kinds of environmental stresses, whereas Thermusspecies have acquired genes from thermophilic bacteria toadapt to high-temperature environments [11].

The distribution of lysine biosynthetic genes in theDeinococcus-Thermus phylum has not been clearly described.In this study, we compared the distribution of the genesfor lysine biosynthesis between 13 organisms (D. deserti,D. geothermalis, D. maricopensis, D. proteolyticus, D. radio-durans, Marinithermus hydrothermalis, Meiothermus ruber,M. silvanus, Oceanithermus profundus, T. scotoductus, T.thermophilus HB8, T. thermophilus HB27, and Trueperaradiovictrix).

2. Methods

We analyzed the distribution of each of the following10 enzymes related to lysine biosynthesis through theAAA pathway in the Deinococcus-Thermus phylum: α-aminoadipate aminotransferase, homoisocitrate dehydro-genase, LysW-γ-l-lysine aminotransferase, LysW-γ-l-lysine

2 International Journal of Evolutionary Biology

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International Journal of Evolutionary Biology 3

Table 2: Genes for lysine biosynthesis through the diaminopimelate pathway in the Deinococcus-Thermus phylum.

OrganismAspartate

kinase

Aspartate-semialdehyde

dehydrogenase

Dihydrodipicolinatesynthase

Dihydrodipicolinatereductase

ll-diaminopimelateaminotransferase

Diaminopimelatedecarboxylase

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

Marinithermushydrothermalis

Marky 1492 Marky 1381 Marky 1261

Deinococcus radiodurans DR 1365 DR 2008 DR 1758

Deinococcus geothermalis Dgeo 1127 Dgeo 1782 Dgeo 0790

Deinococcus deserti Deide 11430 Deide 15740Deide 1p00310,Deide 3p00120,Deide 3p01100

Deide 12830,Deide 21880

Deinococcus maricopensis Deima 1822 Deima 2680 Deima 2660

Deinococcus proteolyticus Deipr 0941 Deipr 0985 Deipr 1377∗ Deipr 1378∗ Deipr 1376∗Deipr 0627,Deipr 1375∗

Truepera radiovictrix Trad 0977 Trad 0289 Trad 1893 Trad 0134∗

More than 3 genes are clustered.

Spirochaeta thermophila STHERM c00170

Denitrovibrio acetiphilus Dacet 0798

Spirochaeta caldaria DSM 7334 Spica 0951

Treponema primitia TREPR 1186

Calditerrivibrio nitroreducens Calni 0514

Flexistipes sinusarabici Flexsi 1574

Methanohalophilus mahii Mmah 0892

Methanococcoides burtonii Mbur 0628

Methanosarcina barkeri Mbar A1641

Methanosarcina mazei MM 1885

Methanosarcina acetivorans MA0726

Selenomonas sputigena Selsp 2045

Syntrophobotulus glycolicus Sgly 1852

Desulfitobacterium hafniense DCB-2 Dhaf 4876Desulfitobacterium hafniense Y51 DSY4977

Spirochaeta smaragdinae Spirs 1460

Deinococcus proteolyticus Deipr 1375

Kytococcus sedentarius Ksed 00760

Spirochaeta sp. Buddy SpiBuddy 1124

Spirochaeta coccoides Spico 0777

33

16

35

35

98

5661

100

0.1

100

89

97

100

100100

100

100

100

Figure 1: Phylogenetic relationship between Deinococcus proteolyticus diaminopimelate decarboxylase and related proteins. Multiplealignment was obtained using the top 20 amino acid sequences of the BLASTp search result for D. proteolyticus diaminopimelatedecarboxylase (Deipro 1375), as based on the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. The maximum-likelihoodtree was constructed using MEGA software version 5 [12]. The WAG model was used as the amino acid substitution model. The nearestneighbor interchange was used for the maximum-likelihood heuristic method. The γ-distributed rate was considered, and the number ofdiscrete γ categories was 3. Bootstrap analysis was performed with 100 replicates. Red indicates D. proteolyticus.


Anabaena variabilis Ava 2354

Anabaena sp. PCC7120 alr5103

Cyanothece sp. PCC 7425 Cyan7425 4424

Acaryochloris marina AM1 1880

Synechococcus elongatus PCC7942 Synpcc7942 0853Synechococcus elongatus PCC6301 syc0687 c

Synechococcus sp. CC9605 Syncc9605 0311

Opitutus terrae Oter 4620

Pelobacter carbinolicus Pcar 2423

Geobacter sp. M21 GM21 4142

Geobacter bemidjiensis Gbem 4052

Geobacter metallireducens Gmet 0213

Geobacter uraniumreducens Gura 0238

Geobacter sp. FRC-32 Geob 1134

Geobacter lovleyi Glov 3040






10059

81

89

87

72

100

100100

94

10074

50

100

100

58

99

0.1

Figure 2: Phylogenetic relationship between Deinococcus proteolyticus ll-diaminopimelate aminotransferase and related proteins. Multiplealignment was obtained using the top 20 amino acid sequences of the BLASTp search result for D. proteolyticus ll-diaminopimelateaminotransferase (Deipro 1376), as based on the KEGG database. The maximum-likelihood tree was constructed using MEGA softwareversion 5 [12]. The WAG model was used as the amino acid substitution model. The nearest neighbor interchange was used for themaximum-likelihood heuristic method. The γ-distributed rate was considered, and the number of discrete γ categories was 3. Bootstrapanalysis was performed with 100 replicates. Red indicates D. proteolyticus.

Desulfovibrio vulgaris DP4 Dvul 1296Desulfovibrio vulgaris Hildenborough DVU1868

Desulfovibrio vulgaris Miyazaki F DvMF 0562

Desulfovibrio desulfuricans G20 Dde 1797

Desulfomicrobium baculatum Dbac 0647

Desulfohalobium retbaense Dret 1874

Desulfovibrio salexigens Desal 1588

Candidatus Nitrospira defluvii NIDE0489

Desulfurivibrio alkaliphilus DaAHT2 2217

Deferribacter desulfuricans SSM1 DEFDS 0215

Calditerrivibrio nitroreducens Calni 1811


Uncultured Termite bacterium phylotype Rs-D17 TGRD 641

Aquifex aeolicus aq 1143

Hydrogenobacter thermophilus HTH 1231






10099

67

72

100

50

67

76

70

94

3550

100

100

5559

100

0.1

Figure 3: Phylogenetic relationship between Deinococcus proteolyticus dihydrodipicolinate synthase and related proteins. Multiple alignmentwas obtained using the top 20 amino acid sequences of the BLASTp search result for D. proteolyticus dihydrodipicolinate synthase (Deipro1377), as based on the KEGG database. The maximum-likelihood tree was constructed using MEGA software version 5 [12]. The WAGmodel was used as the amino acid substitution model. The nearest neighbor interchange was used for the maximum-likelihood heuristicmethod. The γ-distributed rate was considered, and the number of discrete γ categories was 3. Bootstrap analysis was performed with 100replicates. Red indicates D. proteolyticus.

International Journal of Evolutionary Biology 5

Pedobacter heparinus Phep 3529

Pedobacter saltans Pedsa 0258

Muricauda ruestringensis Murru 0253

Leadbetterella byssophila Lbys 0935

Waddlia chondrophila wcw 0766

Parachlamydia acanthamoebae PUV 02330

Candidatus Protochlamydia amoebophila pc0687

Spirochaeta caldaria DSM 7334 Spica 0948

Treponema azotonutricium TREAZ 1304

Treponema primitia TREPR 2975

Treponema succinifaciens Tresu 2067

Chlorobaculum parvum NCIB 8327 Cpar 0353


Rhodothermus marinus DSM 4252 Rmar 1657Rhodothermus marinus SG0.5JP17-172 Rhom172 1129

Salinibacter ruber SRM 01279





88

100

49

24

48

52

5037

45

93

7551

9782

36

97

0.1

100

Figure 4: Phylogenetic relationship between Deinococcus proteolyticus dihydrodipicolinate reductase and related proteins. Multiplealignment was obtained using the top 20 amino acid sequences of the BLASTp search result for D. proteolyticus dihydrodipicolinate reductase(Deipro 1378), as based on the KEGG database. The maximum-likelihood tree was constructed using MEGA software version 5 [12]. TheWAG model was used as the amino acid substitution model. The nearest neighbor interchange was used for the maximum-likelihoodheuristic method. The γ-distributed rate was considered, and the number of discrete γ categories was 3. Bootstrap analysis was performedwith 100 replicates. Red indicates D. proteolyticus.

hydrolase, LysW-γ-l-α-aminoadipate kinase, LysW-γ-l-α-aminoadipyl-6-phosphate reductase, α-aminoadipate-LysWligase LysX, LysU, LysT, and homocitrate synthase. Inaddition, we analyzed the distribution of each of thefollowing 6 enzymes related to lysine biosynthesis throughthe DAP pathway: aspartate kinase, aspartate-semialdehydedehydrogenase, dihydrodipicolinate synthase, dihydrodipi-colinate reductase, ll-diaminopimelate aminotransferase,and diaminopimelate decarboxylase.

Homologous genes were selected on the basis of BLASTpsearch results by using each T. thermophilus enzyme forlysine biosynthesis through the AAA pathway and eachD. proteolyticus enzyme for lysine biosynthesis through theDAP pathway. Multiple alignments were obtained using 20amino acid sequences, with the highest to the 20th highestscore by the BLASTp result. Maximum-likelihood treeswere constructed using MEGA software version 5 [12]. TheWAG model [13] was used as the amino acid substitutionmodel. The nearest neighbor interchange was used for themaximum-likelihood heuristic method. The γ-distributedrate was considered, and the number of discrete γ categorieswas 3. Bootstrap analysis was performed with 100 replicates.

3. Results and Discussion

Genes homologous to the T. thermophilus genes forlysine biosynthesis through the AAA pathway were found

to be widely distributed in bacteria belonging to theDeinococcus-Thermus phylum, except for D. proteolyticus(Table 1). Among the 13 organisms examined, Marinither-mus, Oceanithermus, and Truepera have the largest genecluster, containing 8 lysine biosynthetic genes (Table 1).In each phylogenetic analysis of the 10 enzymes, lysinebiosynthetic genes of the Deinococcus-Thermus phylumwere found to have a common ancestor (See in Sup-plementary Material Figures S1−S10 available online atdoi:10.1155/2012/745931). We hypothesize that a commonancestor of the Deinococcus-Thermus phylum biosynthesizedlysine through the AAA pathway.

In contrast, the distribution of genes for lysine biosyn-thesis through the DAP pathway was found to be limitedin the Deinococcus-Thermus phylum (Table 2). Thus, ll-diaminopimelate aminotransferase and dihydrodipicolinatereductase were identified in no bacteria other than D. prote-olyticus (Table 2). This observation supports our hypothesisthat a common ancestor of the Deinococcus-Thermus phylumbiosynthesized lysine not through the DAP pathway, butthrough the AAA pathway.

Interestingly, D. proteolyticus was found to have thegenes for lysine biosynthesis through the DAP pathway(Table 2). D. proteolyticus has 2 diaminopimelate decar-boxylases, namely, Deipro 0627 and Deipro 1375 (Table 2),which are structurally different from each other. BecauseDeipro 1375 forms a gene cluster with other genes for lysine


biosynthesis through the DAP pathway, we used Deipro1375 as a query sequence in the BLASTp search. Eachphylogenetic tree based on diaminopimelate decarboxylase(Figure 1), ll-diaminopimelate aminotransferase (Figure 2),dihydrodipicolinate synthase (Figure 3), and dihydrodipi-colinate reductase (Figure 4) showed that the D. prote-olyticus enzyme is closely related to that of the generaKytococcus (a member of Actinobacteria) and Spirochaeta(a member of Spirochaetes) (Figures 1−4). The 3 phylaActinobacteria, Deinococcus-Thermus, and Spirochaetes donot form a monophyletic lineage in the phylogenetic tree, asbased on genomewide comparative studies [14]. In addition,the 4 genes encoding diaminopimelate decarboxylase, ll-diaminopimelate aminotransferase, dihydrodipicolinate syn-thase, and dihydrodipicolinate reductase are clustered in eachgenus (Figures 1−4). Thus, these findings strongly suggestedthat a DNA fragment including the 4 D. proteolyticus geneswas horizontally transferred from a phylogenetically distantorganism. This horizontal transfer event may have inducedthe loss of the genes for lysine biosynthesis through the AAApathway in D. proteolyticus.

References

[1] W. G. Weisburg, S. J. Giovannoni, and C. R. Woese, “TheDeinococcus-Thermus phylum and the effect of rRNA com-position on phylogenetic tree construction,” Systematic andApplied Microbiology, vol. 11, pp. 128–134, 1989.

[2] E. Griffiths and R. S. Gupta, “Distinctive protein signaturesprovide molecular markers and evidence for the monophyleticnature of the Deinococcus-Thermus phylum,” Journal of Bacte-riology, vol. 186, no. 10, pp. 3097–3107, 2004.

[3] M. Kanehisa, S. Goto, Y. Sato, M. Furumichi, and M.Tanabe, “KEGG for integration and interpretation of large-scale molecular datasets,” Nucleic Acids Research, vol. 40, pp.D109–D114, 2012.

[4] H. Nishida, R. Abe, T. Nagayama, and K. Yano, “Genomesignature difference between Deinococcus radiodurans andThermus thermopilus,” International Journal of EvolutionaryBiology, vol. 2012, Article ID 205274, 6 pages, 2012.

[5] A. M. Velasco, J. I. Leguina, and A. Lazcano, “Molecularevolution of the lysine biosynthetic pathways,” Journal ofMolecular Evolution, vol. 55, no. 4, pp. 445–459, 2002.

[6] H. Nishida, M. Nishiyama, N. Kobashi, T. Kosuge, T. Hoshino,and H. Yamane, “A prokaryotic gene cluster involved insynthesis of lysine through the amino adipate pathway: a keyto the evolution of amino acid biosynthesis,” Genome Research,vol. 9, no. 12, pp. 1175–1183, 1999.

[7] T. Kosuge and T. Hoshino, “Lysine is synthesized throughthe α-aminoadipate pathway in Thermus thermophilus,” FEMSMicrobiology Letters, vol. 169, no. 2, pp. 361–367, 1998.

[8] N. Kobashi, M. Nishiyama, and M. Tanokura, “Aspartatekinase-independent lysine synthesis in an extremely ther-mophilic bacterium, Thermus thermophilus: lysine is synthe-sized via α-aminoadipic acid not via diaminopimelic acid,”Journal of Bacteriology, vol. 181, no. 6, pp. 1713–1718, 1999.

[9] H. Nishida, “Distribution of genes for lysine biosynthe-sis through the aminoadipate pathway among prokaryoticgenomes,” Bioinformatics, vol. 17, no. 2, pp. 189–191, 2001.

[10] H. Nishida and I. Narumi, “Phylogenetic and disruptionanalyses of aspartate kinase of Deinococcus radiodurans,”

Bioscience, Biotechnology and Biochemistry, vol. 71, no. 4, pp.1015–1020, 2007.

[11] M. V. Omelchenko, Y. I. Wolf, E. K. Gaidamakova et al., “Com-parative genomics of Thermus thermophilus and Deinococcusradiodurans: divergent routes of adaptation to thermophilyand radiation resistance,” BMC Evolutionary Biology, vol. 5,article 57, 2005.

[12] K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei,and S. Kumar, “MEGA5: molecular evolutionary geneticsanalysis using maximum likelihood, evolutionary distance,and maximum parsimony methods,” Molecular Biology andEvolution, vol. 28, no. 10, pp. 2731–2739, 2011.

[13] S. Whelan and N. Goldman, “A general empirical modelof protein evolution derived from multiple protein familiesusing a maximum-likelihood approach,” Molecular Biologyand Evolution, vol. 18, no. 5, pp. 691–699, 2001.

[14] H. Nishida, T. Beppu, and K. Ueda, “Whole-genome compari-son clarifies close phylogenetic relationships between the phylaDictyoglomi and Thermotogae,” Genomics, vol. 98, no. 5, pp.370–375, 2011.

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