The Suf iron-sulfur cluster biosynthetic system is essential in Staphylococcus aureus, and decreased Suf function results in global metabolic defects and reduced survival in human neutrophils

Infection and Immunity

Volumn 85, Issue 6, 2017, Pages

  Roberts, Christina A ^a   Al Tameemi, Hassan M ^a   Mashruwala, Ameya A ^a   Rosario Cruz, Zuelay ^a   Chauhan, Unnati ^a   Sause, William E ^b   Torres, Victor J ^b   Belden, William J ^c   Boyd, Jeffrey M ^a  

^a The State University of New Jersey   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Cluster; Iron; Neutrophil; Staphylococcus aureus; Suf; Sulfur

Indexed keywords

IRON SULFUR PROTEIN; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SIGMA FACTOR; TRICARBOXYLIC ACID; BACTERIAL PROTEIN; COMPLEMENTARY RNA; OXYGEN;

ANIMAL MODEL; ARTICLE; BIOSYNTHESIS; CELL METABOLISM; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; HUMAN; HUMAN CELL; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; RNA TRANSCRIPTION; STAPHYLOCOCCUS AUREUS; TRANSPOSON; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; STAPHYLOCOCCUS INFECTION; VIRULENCE;

BACTERIAL PROTEINS; HUMANS; IRON-SULFUR PROTEINS; NEUTROPHILS; OXYGEN; REACTIVE NITROGEN SPECIES; RNA, ANTISENSE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE;

EID: 85019952880     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00100-17     Document Type: Article

References (99)

1. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK. 2007. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771. https://doi.org/10.1001/jama.298.15.1763
2. Daum RS. 2007. Clinical practice. Skin and soft-tissue infections caused by methicillin-resistant Staphylococcus aureus. N Engl J Med 357: 380-390
3. Lodise TP, Jr, McKinnon PS. 2007. Burden of methicillin-resistant Staphylococcus aureus: focus on clinical and economic outcomes. Pharmacotherapy 27:1001-1012. https://doi.org/10.1592/phco.27.7.1001
4. Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y. 2003. Comparison of mortality associated with methicillinresistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 36:53-59. https://doi.org/10.1086/345476
5. Lewis K. 2013. Platforms for antibiotic discovery. Nat Rev Drug Discov 12:371-387. https://doi.org/10.1038/nrd3975
6. Skaar EP, Humayun M, Bae T, DeBord KL, Schneewind O. 2004. Ironsource preference of Staphylococcus aureus infections. Science 305: 1626-1628. https://doi.org/10.1126/science.1099930
7. Mashruwala AA, Pang YY, Rosario-Cruz Z, Chahal HK, Benson MA, Mike LA, Skaar EP, Torres VJ, Nauseef WM, Boyd JM. 2015. Nfu facilitates the maturation of iron-sulfur proteins and participates in virulence in Staphylococcus aureus. Mol Microbiol 95:383-409. https://doi.org/10.1111/mmi.12860
8. Zheng L, Cash VL, Flint DH, Dean DR. 1998. Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273:13264-13272
9. Yuvaniyama P, Agar JN, Cash VL, Johnson MK, Dean DR. 2000. NifSdirected assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc Natl Acad Sci U S A 97:599-604. https://doi.org/10.1073/pnas.97.2.599
10. Takahashi Y, Tokumoto U. 2002. A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J Biol Chem 277:28380-28393. https://doi.org/10.1074/jbc. C200365200
11. Wollers S, Layer G, Garcia-Serres R, Signor L, Clemancey M, Latour JM, Fontecave M, Ollagnier de Choudens S. 2010. Iron-sulfur (Fe-S) cluster assembly: the SufBCD complex is a new type of Fe-S scaffold with a flavin redox cofactor. J Biol Chem 285:23331-23341. https://doi.org/10.1074/jbc. M110.127449
12. Nachin L, El Hassouni M, Loiseau L, Expert D, Barras F. 2001. SoxRdependent response to oxidative stress and virulence of Erwinia chrysanthemi: the key role of SufC, an orphan ABC ATPase. Mol Microbiol 39:960-972. https://doi.org/10.1046/j.1365-2958.2001.02288.x
13. Saini A, Mapolelo DT, Chahal HK, Johnson MK, Outten FW. 2010. SufD and SufC ATPase activity are required for iron acquisition during in vivo Fe-S cluster formation on SufB. Biochemistry 49:9402-9412. https://doi.org/10.1021/bi1011546
14. Layer G, Gaddam SA, Ayala-Castro CN, Ollagnier-de Choudens S, Lascoux D, Fontecave M, Outten FW. 2007. SufE transfers sulfur from SufS to SufB for iron-sulfur cluster assembly. J Biol Chem 282:13342-13350. https://doi.org/10.1074/jbc. M608555200
15. Selbach B, Earles E, Dos Santos PC. 2010. Kinetic analysis of the bisubstrate cysteine desulfurase SufS from Bacillus subtilis. Biochemistry 49: 8794-8802. https://doi.org/10.1021/bi101358k
16. Selbach BP, Chung AH, Scott AD, George SJ, Cramer SP, Dos Santos PC. 2014. Fe-S cluster biogenesis in Gram-positive bacteria: SufU is a zincdependent sulfur transfer protein. Biochemistry 53:152-160. https://doi.org/10.1021/bi4011978
17. Chahal HK, Outten FW. 2012. Separate FeS scaffold and carrier functions for SufB(2)C(2) and SufA during in vitro maturation of [2Fe2S] Fdx. J Inorg Biochem 116:126-134. https://doi.org/10.1016/j.jinorgbio.2012.06.008
18. Rosario-Cruz Z, Chahal HK, Mike LA, Skaar EP, Boyd JM. 2015. Bacillithiol has a role in Fe-S cluster biogenesis in Staphylococcus aureus. Mol Microbiol 98:218-242. https://doi.org/10.1111/mmi.13115
19. Mashruwala AA, Bhatt S, Poudel S, Boyd ES, Boyd JM. 2016. The DUF59 containing protein SufT is involved in the maturation of iron-sulfur (FeS) proteins during conditions of high FeS cofactor demand in Staphylococcus aureus. PLoS Genet 12:e1006233. https://doi.org/10.1371/journal.pgen.1006233
20. Rosario-Cruz Z, Boyd JM. 2016. Physiological roles of bacillithiol in intracellular metal processing. Curr Genet 62:59-65. https://doi.org/10.1007/s00294-015-0511-0
21. Lill R. 2009. Function and biogenesis of iron-sulphur proteins. Nature 460:831-838. https://doi.org/10.1038/nature08301
22. Valentino MD, Foulston L, Sadaka A, Kos VN, Villet RA, Santa Maria J, Jr, Lazinski DW, Camilli A, Walker S, Hooper DC, Gilmore MS. 2014. Genes contributing to Staphylococcus aureus fitness in abscess-and infectionrelated ecologies. mBio 5:e01729-01714. https://doi.org/10.1128/mBio.01729-14
23. Santiago M, Matano LM, Moussa SH, Gilmore MS, Walker S, Meredith TC. 2015. A new platform for ultra-high density Staphylococcus aureus transposon libraries. BMC Genomics 16:252. https://doi.org/10.1186/s12864-015-1361-3
24. Chaudhuri RR, Allen AG, Owen PJ, Shalom G, Stone K, Harrison M, Burgis TA, Lockyer M, Garcia-Lara J, Foster SJ, Pleasance SJ, Peters SE, Maskell DJ, Charles IG. 2009. Comprehensive identification of essential Staphylococcus aureus genes using transposon-mediated differential hybridisation (TMDH). BMC Genomics 10:291. https://doi.org/10.1186/1471-2164-10-291
25. Ji Y, Woodnutt G, Rosenberg M, Burnham MK. 2002. Identification of essential genes in Staphylococcus aureus using inducible antisense RNA. Methods Enzymol 358:123-128. https://doi.org/10.1016/S0076-6879(02)58084-8
26. Traber K, Novick R. 2006. A slipped-mispairing mutation in AgrA of laboratory strains and clinical isolates results in delayed activation of agr and failure to translate delta-and alpha-haemolysins. Mol Microbiol 59:1519-1530. https://doi.org/10.1111/j.1365-2958.2006.04986.x
27. Nair D, Memmi G, Hernandez D, Bard J, Beaume M, Gill S, Francois P, Cheung AL. 2011. Whole-genome sequencing of Staphylococcus aureus strain RN4220, a key laboratory strain used in virulence research, identifies mutations that affect not only virulence factors but also the fitness of the strain. J Bacteriol 193:2332-2335. https://doi.org/10.1128/JB.00027-11
28. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, Bayles KW. 2013. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio 4:e00537-00512. https://doi.org/10.1128/mBio.00537-12
29. Osmundson J, Dewell S, Darst SA. 2013. RNA-Seq reveals differential gene expression in Staphylococcus aureus with single-nucleotide resolution. PLoS One 8:e76572. https://doi.org/10.1371/journal.pone.0076572
30. Pane-Farre J, Jonas B, Forstner K, Engelmann S, Hecker M. 2006. The sigmaB regulon in Staphylococcus aureus and its regulation. Int J Med Microbiol 296:237-258. https://doi.org/10.1016/j.ijmm.2005.11.011
31. Gertz S, Engelmann S, Schmid R, Ziebandt AK, Tischer K, Scharf C, Hacker J, Hecker M. 2000. Characterization of the sigma(B) regulon in Staphylococcus aureus. J Bacteriol 182:6983-6991. https://doi.org/10.1128/JB.182.24.6983-6991.2000
32. Kennedy MC, Emptage MH, Dreyer JL, Beinert H. 1983. The role of iron in the activation-inactivation of aconitase. J Biol Chem 258:11098-11105
33. Mashruwala AA, Boyd JM. 2017. The Staphylococcus aureus SrrAB regulatory system modulates hydrogen peroxide resistance factors, which imparts protection to aconitase during aerobic growth. PLoS One 12: e0170283. https://doi.org/10.1371/journal.pone.0170283
34. Ledala N, Zhang B, Seravalli J, Powers R, Somerville GA. 2014. Influence of iron and aeration on Staphylococcus aureus growth, metabolism, and transcription. J Bacteriol 196:2178-2189. https://doi.org/10.1128/JB.01475-14
35. Vanoni MA, Curti B. 2008. Structure-function studies of glutamate synthases: a class of self-regulated iron-sulfur flavoenzymes essential for nitrogen assimilation. IUBMB Life 60:287-300. https://doi.org/10.1002/iub.52
36. Ollagnier-de Choudens S, Fontecave M. 1999. The lipoate synthase from Escherichia coli is an iron-sulfur protein. FEBS Lett 453:25-28. https://doi.org/10.1016/S0014-5793(99)00694-8
37. Flint DH, Emptage MH. 1988. Dihydroxy acid dehydratase from spinach contains a [2Fe-2S] cluster. J Biol Chem 263:3558-3564
38. Hentze MW, Argos P. 1991. Homology between IRE-BP, a regulatory RNA-binding protein, aconitase, and isopropylmalate isomerase. Nucleic Acids Res 19:1739-1740. https://doi.org/10.1093/nar/19.8.1739
39. Miller RE. 1974. Glutamate synthase from Escherichia coli-an iron-sulfur flavoprotein. Separation and analysis of non-identical subunits. Biochim Biophys Acta 364:243-249
40. Porello SL, Cannon MJ, David SS. 1998. A substrate recognition role for the [4Fe-4S]2+ cluster of the DNA repair glycosylase MutY. Biochemistry 37:6465-6475. https://doi.org/10.1021/bi972433t
41. Fu W, O'Handley S, Cunningham RP, Johnson MK. 1992. The role of the iron-sulfur cluster in Escherichia coli endonuclease III. A resonance Raman study. J Biol Chem 267:16135-16137
42. Yeeles JT, Cammack R, Dillingham MS. 2009. An iron-sulfur cluster is essential for the binding of broken DNA by AddAB-type helicasenucleases. J Biol Chem 284:7746-7755. https://doi.org/10.1074/jbc.M808526200
43. Ezekiel DH, Hutchins JE. 1968. Mutations affecting RNA polymerase associated with rifampicin resistance in Escherichia coli. Nature 220: 276-277. https://doi.org/10.1038/220276a0
44. Jang S, Imlay JA. 2007. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J Biol Chem 282:929-937. https://doi.org/10.1074/jbc. M607646200
45. Duan X, Yang J, Ren B, Tan G, Ding H. 2009. Reactivity of nitric oxide with the [4Fe-4S] cluster of dihydroxyacid dehydratase from Escherichia coli. Biochem J 417:783-789. https://doi.org/10.1042/BJ20081423
46. Grossi L, D'Angelo S. 2005. Sodium nitroprusside: mechanism of NO release mediated by sulfhydryl-containing molecules. J Med Chem 48: 2622-2626. https://doi.org/10.1021/jm049857n
47. Rauen U, Springer A, Weisheit D, Petrat F, Korth HG, de Groot H, Sustmann R. 2007. Assessment of chelatable mitochondrial iron by using mitochondrion-selective fluorescent iron indicators with different ironbinding affinities. Chembiochem 8:341-352. https://doi.org/10.1002/cbic.200600311
48. Speziali CD, Dale SE, Henderson JA, Vines ED, Heinrichs DE. 2006. Requirement of Staphylococcus aureus ATP-binding cassette-ATPase FhuC for iron-restricted growth and evidence that it functions with more than one iron transporter. J Bacteriol 188:2048-2055. https://doi.org/10.1128/JB.188.6.2048-2055.2006
49. Bolzan AD, Bianchi MS. 2001. Genotoxicity of streptonigrin: a review. Mutat Res 488:25-37. https://doi.org/10.1016/S1383-5742(00)00062-4
50. White JR, Yeowell HN. 1982. Iron enhances the bactericidal action of streptonigrin. Biochem Biophys Res Commun 106:407-411. https://doi.org/10.1016/0006-291X(82)91125-1
51. DeGraffW, Hahn SM, Mitchell JB, Krishna MC. 1994. Free radical modes of cytotoxicity of adriamycin and streptonigrin. Biochem Pharmacol 48:1427-1435. https://doi.org/10.1016/0006-2952(94)90567-3
52. Bartlett AH, Hulten KG. 2010. Staphylococcus aureus pathogenesis: secretion systems, adhesins, and invasins. Pediatr Infect Dis J 29:860-861. https://doi.org/10.1097/INF.0b013e3181ef2477
53. Recsei P, Kreiswirth B, O'Reilly M, Schlievert P, Gruss A, Novick RP. 1986. Regulation of exoprotein gene expression in Staphylococcus aureus by agar. Mol Gen Genet 202:58-61. https://doi.org/10.1007/BF00330517
54. Otto M. 2008. Staphylococcal biofilms. Curr Top Microbiol Immunol 322:207-228
55. Lauderdale KJ, Boles BR, Cheung AL, Horswill AR. 2009. Interconnections between sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect Immun 77:1623-1635. https://doi.org/10.1128/IAI.01036-08
56. Boles BR, Horswill AR. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052. https://doi.org/10.1371/journal.ppat.1000052
57. Nauseef WM. 2007. How human neutrophils kill and degrade microbes: an integrated view. Immunol Rev 219:88-102. https://doi.org/10.1111/j.1600-065X.2007.00550.x
58. Boyd ES, Thomas KM, Dai Y, Boyd JM, Outten FW. 2014. Interplay between oxygen and Fe-S cluster biogenesis: insights from the Suf pathway. Biochemistry 53:5834-5847. https://doi.org/10.1021/bi500488r
59. Py B, Barras F. 2010. Building Fe-S proteins: bacterial strategies. Nat Rev Microbiol 8:436-446. https://doi.org/10.1038/nrmicro2356
60. Bachman MA, Breen P, Deornellas V, Mu Q, Zhao L, Wu W, Cavalcoli JD, Mobley HL. 2015. Genome-wide identification of Klebsiella pneumoniae fitness genes during lung infection. mBio 6:e00775. https://doi.org/10.1128/mBio.00775-15
61. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006 0008. https://doi.org/10.1038/msb4100050
62. Flint DH, Tuminello JF, Emptage MH. 1993. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem 268: 22369-22376
63. Mashruwala AA, Roberts CA, Bhatt S, May KL, Carroll RK, Shaw LN, Boyd JM. 2016. Staphylococcus aureus SufT: an essential iron-sulfur cluster assembly factor in cells experiencing a high demand for lipoic acid. Mol Microbiol 102:1099-1119. https://doi.org/10.1111/mmi.13539
64. Pang YY, Schwartz J, Bloomberg S, Boyd JM, Horswill AR, Nauseef WM. 2014. Methionine sulfoxide reductases protect against oxidative stress in Staphylococcus aureus encountering exogenous oxidants and human neutrophils. J Innate Immun 6:353-364. https://doi.org/10.1159/000355915
65. Novick RP. 1963. Analysis by transduction of mutations affecting penicillinase formation in Staphylococcus aureus. J Gen Microbiol 33:121-136. https://doi.org/10.1099/00221287-33-1-121
66. Eidem TM, Lounsbury N, Emery JF, Bulger J, Smith A, Abou-Gharbia M, Childers W, Dunman PM. 2015. Small-molecule inhibitors of Staphylococcus aureus RnpA-mediated RNA turnover and tRNA processing. Antimicrob Agents Chemother 59:2016-2028. https://doi.org/10.1128/AAC.04352-14
67. Lei MG, Cue D, Roux CM, Dunman PM, Lee CY. 2011. Rsp inhibits attachment and biofilm formation by repressing fnbA in Staphylococcus aureus MW2. J Bacteriol 193:5231-5241. https://doi.org/10.1128/JB.05454-11
68. Joska TM, Mashruwala A, Boyd JM, Belden WJ. 2014. A universal cloning method based on yeast homologous recombination that is simple, efficient, and versatile. J Microbiol Methods 100:46-51. https://doi.org/10.1016/j.mimet.2013.11.013
69. Mashruwala AA, Boyd JM. 2016. De novo assembly of plasmids using yeast recombinational cloning. Methods Mol Biol 1373:33-41. https://doi.org/10.1007/7651_2015_275
70. Trapnell C, Roberts A, GoffL, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562-578. https://doi.org/10.1038/nprot.2012.016
71. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511-515. https://doi.org/10.1038/nbt.1621
72. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079. https://doi.org/10.1093/bioinformatics/btp352
73. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat Biotechnol 29: 24-26. https://doi.org/10.1038/nbt.1754
74. Dougall DK. 1974. Evidence for the presence of glutamate synthase in extracts of carrot cell cultures. Biochem Biophys Res Commun 58: 639-646. https://doi.org/10.1016/S0006-291X(74)80466-3
75. Olson BJ, Markwell J. 2007. Assays for determination of protein concentration. Curr Protoc Protein Sci Chapter 3:Unit 3.4
76. Blevins JS, Beenken KE, Elasri MO, Hurlburt BK, Smeltzer MS. 2002. Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect Immun 70:470-480. https://doi.org/10.1128/IAI.70.2.470-480.2002
77. DuMont AL, Yoong P, Surewaard BG, Benson MA, Nijland R, van Strijp JA, Torres VJ. 2013. Staphylococcus aureus elaborates leukocidin AB to mediate escape from within human neutrophils. Infect Immun 81: 1830-1841. https://doi.org/10.1128/IAI.00095-13
78. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
79. Boles BR, Thoendel M, Roth AJ, Horswill AR. 2010. Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS One 5:e10146. https://doi.org/10.1371/journal.pone.0010146
80. Sadykov MR, Mattes TA, Luong TT, Zhu Y, Day SR, Sifri CD, Lee CY, Somerville GA. 2010. Tricarboxylic acid cycle-dependent synthesis of Staphylococcus aureus type 5 and 8 capsular polysaccharides. J Bacteriol 192:1459-1462. https://doi.org/10.1128/JB.01377-09
81. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712. https://doi.org/10.1038/305709a0
82. Luong TT, Lee CY. 2007. Improved single-copy integration vectors for Staphylococcus aureus. J Microbiol Methods 70:186-190. https://doi.org/10.1016/j.mimet.2007.04.007
83. Gallagher LA, Ramage E, Weiss EJ, Radey M, Hayden HS, Held KG, Huse HK, Zurawski DV, Brittnacher MJ, Manoil C. 2015. Resources for genetic and genomic analysis of emerging pathogen Acinetobacter baumannii. J Bacteriol 197:2027-2035. https://doi.org/10.1128/JB.00131-15
84. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, Arnaud M, Asai K, Ashikaga S, Aymerich S, Bessieres P, Boland F, Brignell SC, Bron S, Bunai K, Chapuis J, Christiansen LC, Danchin A, Debarbouille M, Dervyn E, Deuerling E, Devine K, Devine SK, Dreesen O, Errington J, Fillinger S, Foster SJ, Fujita Y, Galizzi A, Gardan R, Eschevins C, Fukushima T, Haga K, Harwood CR, Hecker M, Hosoya D, Hullo MF, Kakeshita H, Karamata D, Kasahara Y, Kawamura F, Koga K, Koski P, Kuwana R, Imamura D, Ishimaru M, Ishikawa S, Ishio I, Le Coq D, Masson A, Mauel C, Meima R, Mellado RP, Moir A, Moriya S, Nagakawa E, Nanamiya H, Nakai S, Nygaard P, Ogura M, Ohanan T, O'Reilly M, O'Rourke M, Pragai Z, Pooley HM, Rapoport G, Rawlins JP, Rivas LA, Rivolta C, Sadaie A, Sadaie Y, Sarvas M, Sato T, Saxild HH, Scanlan E, Schumann W, Seegers JF, Sekiguchi J, Sekowska A, Séror SJ, Simon M, Stragier P, Studer R, Takamatsu H, Tanaka T, Takeuchi M, Thomaides HB, Vagner V, van Dijl JM, Watabe K, Wipat A, Yamamoto H, Yamamoto M, Yamamoto Y, Yamane K, Yata K, Yoshida K, Yoshikawa H, Zuber U, Ogasawara N. 2003. Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100:4678-4683. https://doi.org/10.1073/pnas.0730515100
85. Veeranagouda Y, Husain F, Tenorio EL, Wexler HM. 2014. Identification of genes required for the survival of B. fragilis using massive parallel sequencing of a saturated transposon mutant library. BMC Genomics 15:429. https://doi.org/10.1186/1471-2164-15-429
86. Moule MG, Hemsley CM, Seet Q, Guerra-Assuncao JA, Lim J, Sarkar-Tyson M, Clark TG, Tan PB, Titball RW, Cuccui J, Wren BW. 2014. Genome-wide saturation mutagenesis of Burkholderia pseudomallei K96243 predicts essential genes and novel targets for antimicrobial development. mBio 5:e00926-00913. https://doi.org/10.1128/mBio.00926-13
87. Metris A, Reuter M, Gaskin DJ, Baranyi J, van Vliet AH. 2011. In vivo and in silico determination of essential genes of Campylobacter jejuni. BMC Genomics 12:535. https://doi.org/10.1186/1471-2164-12-535
88. Dembek M, Barquist L, Boinett CJ, Cain AK, Mayho M, Lawley TD, Fairweather NF, Fagan RP. 2015. High-throughput analysis of gene essentiality and sporulation in Clostridium difficile. mBio 6:e02383. https://doi.org/10.1128/mBio.02383-14
89. Garsin DA, Urbach J, Huguet-Tapia JC, Peters JE, Ausubel FM. 2004. Construction of an Enterococcus faecalis Tn917-mediated-genedisruption library offers insight into Tn917 insertion patterns. J Bacteriol 186:7280-7289. https://doi.org/10.1128/JB.186.21.7280-7289.2004
90. Gallagher LA, Ramage E, Jacobs MA, Kaul R, Brittnacher M, Manoil C. 2007. A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci U S A 104:1009-1014. https://doi.org/10.1073/pnas.0606713104
91. Akerley BJ, Rubin EJ, Novick VL, Amaya K, Judson N, Mekalanos JJ. 2002. A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc Natl Acad Sci U S A 99: 966-971. https://doi.org/10.1073/pnas.012602299
92. Salama NR, Shepherd B, Falkow S. 2004. Global transposon mutagenesis and essential gene analysis of Helicobacter pylori. J Bacteriol 186: 7926-7935. https://doi.org/10.1128/JB.186.23.7926-7935.2004
93. Huet G, Daffe M, Saves I. 2005. Identification of the Mycobacterium tuberculosis SUF machinery as the exclusive mycobacterial system of [Fe-S] cluster assembly: evidence for its implication in the pathogen's survival. J Bacteriol 187:6137-6146. https://doi.org/10.1128/JB.187.17.6137-6146.2005
94. Klein BA, Tenorio EL, Lazinski DW, Camilli A, Duncan MJ, Hu LT. 2012. Identification of essential genes of the periodontal pathogen Porphyromonas gingivalis. BMC Genomics 13:578. https://doi.org/10.1186/1471-2164-13-578
95. Lee SA, Gallagher LA, Thongdee M, Staudinger BJ, Lippman S, Singh PK, Manoil C. 2015. General and condition-specific essential functions of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 112:5189-5194. https://doi.org/10.1073/pnas.1422186112
96. Knuth K, Niesalla H, Hueck CJ, Fuchs TM. 2004. Large-scale identification of essential Salmonella genes by trapping lethal insertions. Mol Microbiol 51:1729-1744. https://doi.org/10.1046/j.1365-2958.2003.03944.x
97. van Opijnen T, Camilli A. 2012. A fine scale phenotype-genotype virulence map of a bacterial pathogen. Genome Res 22:2541-2551. https://doi.org/10.1101/gr.137430.112
98. Le Breton Y, Belew AT, Valdes KM, Islam E, Curry P, Tettelin H, ShirtliffME, El-Sayed NM, McIver KS. 2015. Essential genes in the core genome of the human pathogen Streptococcus pyogenes. Sci Rep 5:9838. https://doi.org/10.1038/srep09838
99. Kamp HD, Patimalla-Dipali B, Lazinski DW, Wallace-Gadsden F, Camilli A. 2013. Gene fitness landscapes of Vibrio cholerae at important stages of its life cycle. PLoS Pathog 9:e1003800. https://doi.org/10.1371/journal.ppat.1003800