Interplay between Yersinia pestis and its flea vector in lipoate metabolism.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
16
06
2020
accepted:
11
11
2020
revised:
22
10
2020
pubmed:
23
1
2021
medline:
22
4
2021
entrez:
22
1
2021
Statut:
ppublish
Résumé
To thrive, vector-borne pathogens must survive in the vector's gut. How these pathogens successfully exploit this environment in time and space has not been extensively characterized. Using Yersinia pestis (the plague bacillus) and its flea vector, we developed a bioluminescence-based approach and employed it to investigate the mechanisms of pathogenesis at an unprecedented level of detail. Remarkably, lipoylation of metabolic enzymes, via the biosynthesis and salvage of lipoate, increases the Y. pestis transmission rate by fleas. Interestingly, the salvage pathway's lipoate/octanoate ligase LplA enhances the first step in lipoate biosynthesis during foregut colonization but not during midgut colonization. Lastly, Y. pestis primarily uses lipoate provided by digestive proteolysis (presumably as lipoyl peptides) rather than free lipoate in blood, which is quickly depleted by the vector. Thus, spatial and temporal factors dictate the bacterium's lipoylation strategies during an infection, and replenishment of lipoate by digestive proteolysis in the vector might constitute an Achilles' heel that is exploited by pathogens.
Identifiants
pubmed: 33479491
doi: 10.1038/s41396-020-00839-0
pii: 10.1038/s41396-020-00839-0
pmc: PMC8182812
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1136-1149Références
Olive AJ, Sassetti CM. Metabolic crosstalk between host and pathogen: sensing, adapting and competing. Nat Rev Microbiol. 2016;14:221–34.
pubmed: 26949049
doi: 10.1038/nrmicro.2016.12
Passalacqua KD, Charbonneau M-E, O’Riordan MXD. Bacterial metabolism shapes the host-pathogen interface. Microbiol Spectr. 2016;4:VMBF-0027-2015.
doi: 10.1128/microbiolspec.VMBF-0027-2015
Simpson SJ, Clissold FJ, Lihoreau M, Ponton F, Wilder SM, Raubenheimer D. Recent advances in the integrative nutrition of arthropods. Annu Rev Entomol. 2015;60:293–311.
pubmed: 25341097
doi: 10.1146/annurev-ento-010814-020917
Schaible UE, Kaufmann SH. A nutritive view on the host-pathogen interplay. Trends Microbiol. 2005;13:373–80.
pubmed: 15993074
doi: 10.1016/j.tim.2005.06.009
Hacquard S, Garrido-Oter R, González A, Spaepen S, Ackermann G, Lebeis S, et al. Microbiota and host nutrition across plant and animal Kingdoms. Cell Host Microbe. 2015;17:603–16.
pubmed: 25974302
doi: 10.1016/j.chom.2015.04.009
Hu Y, Sanders JG, Łukasik P, D’Amelio CL, Millar JS, Vann DR, et al. Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome. Nat Commun. 2018;9:964.
pubmed: 29511180
pmcid: 5840417
doi: 10.1038/s41467-018-03357-y
Baumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016;535:85–93.
pubmed: 27383983
pmcid: 5114849
doi: 10.1038/nature18849
Coppens I. Targeting lipid biosynthesis and salvage in apicomplexan parasites for improved chemotherapies. Nat Rev Microbiol. 2013;11:823–35.
pubmed: 24162026
doi: 10.1038/nrmicro3139
Yuan Y, Zallot R, Grove TL, Payan DJ, Martin-Verstraete I, Šepić S, et al. Discovery of novel bacterial queuine salvage enzymes and pathways in human pathogens. Proc Natl Acad Sci. 2019;116:19126–35.
pubmed: 31481610
pmcid: 6754566
doi: 10.1073/pnas.1909604116
Bacot AW, Martin CJLXVII. Observations on the mechanism of the transmission of plague by fleas. J Hyg (Lond). 1914;13:423–39.
Sebbane F, Lemaître N, Sturdevant DE, Rebeil R, Virtaneva K, Porcella ST, et al. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc Natl Acad Sci. 2006;103:11766–71.
pubmed: 16864791
pmcid: 1518801
doi: 10.1073/pnas.0601182103
Pradel E, Lemaître N, Merchez M, Ricard I, Reboul A, Dewitte A, et al. New insights into how Yersinia pestis adapts to its mammalian host during bubonic plague. PLoS Pathog. 2014;10:e1004029.
pubmed: 24675805
pmcid: 3968184
doi: 10.1371/journal.ppat.1004029
Vadyvaloo V, Jarett C, Sturdevant DE, Sebbane F, Hinnebusch BJ. Transit through the flea vector induces a pretransmission innate immunity resistance phenotype in Yersinia pestis. PLoS Pathog. 2010;6:e1000783.
pubmed: 20195507
pmcid: 2829055
doi: 10.1371/journal.ppat.1000783
Hinnebusch BJ, Jarrett CO, Bland DM. “Fleaing” the plague: adaptations of yersinia pestis to its insect vector that lead to transmission. Annu Rev Microbiol. 2017;71:215–32.
pubmed: 28886687
doi: 10.1146/annurev-micro-090816-093521
Bontemps-Gallo S, Fernandez M, Dewitte A, Raphaël E, Gherardini FC, Pradel E, et al. Nutrient depletion may trigger the Yersinia pestis OmpR-EnvZ regulatory system to promote flea-borne plague transmission. Mol Microbiol. 2019;112:1471–82.
pubmed: 31424585
pmcid: 6842400
doi: 10.1111/mmi.14372
Dewitte A, Bouvenot T, Pierre F, Ricard I, Pradel E, Barois N, et al. A refined model of how Yersinia pestis produces a transmissible infection in its flea vector. PLoS Pathog. 2020;16:e1008440.
pubmed: 32294143
pmcid: 7185726
doi: 10.1371/journal.ppat.1008440
Hinnebusch BJ, Perry RD, Schwan TG. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science. 1996;273:367–70.
pubmed: 8662526
doi: 10.1126/science.273.5273.367
Sebbane F, Jarett CO, Gardner D, Long D, Hinnebusch BJ. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc Natl Acad Sci. 2006;103:5526–30.
pubmed: 16567636
pmcid: 1414629
doi: 10.1073/pnas.0509544103
Rempe KA, Hinz AK, Vadyvaloo V. Hfq regulates biofilm gut blockage that facilitates flea-borne transmission of Yersinia pestis. J Bacteriol. 2012;194:2036–40.
pubmed: 22328669
pmcid: 3318476
doi: 10.1128/JB.06568-11
Sun YC, Koumouts A, Jarrett C, Lawrence K, Gherardini FC, Darby C, et al. Differential control of Yersinia pestis biofilm formation in vitro and in the flea vector by two c-di-GMP diguanylate cyclases. PLoS ONE. 2011;6:e19267.
pubmed: 21559445
pmcid: 3084805
doi: 10.1371/journal.pone.0019267
Ren G-X, Yan H-Q, Zhu H, Guo X-P, Sun Y-C. HmsC, a periplasmic protein, controls biofilm formation via repression of HmsD, a diguanylate cyclase in Yersinia pestis. Environ Microbiol. 2014;16:1202–16.
pubmed: 24192006
doi: 10.1111/1462-2920.12323
Tam C, Demke O, Hermanas T, Mitchell A, Hendrickx APA, Schneewind O. YfbA, a Yersinia pestis regulator required for colonization and biofilm formation in the gut of cat fleas. J Bacteriol. 2014;196:1165–73.
pubmed: 24391055
pmcid: 3957715
doi: 10.1128/JB.01187-13
Vadyvaloo V, Hinz AK. A LysR-type transcriptional regulator, rovm, senses nutritional cues suggesting that it is involved in metabolic adaptation of Yersinia pestis to the flea gut. PLoS ONE. 2015;10:e0137508.
pubmed: 26348850
pmcid: 4562620
doi: 10.1371/journal.pone.0137508
Darby C, Ananth SL, Tan L, Hinnebusch BJ. Identification of gmhA, a Yersinia pestis gene required for flea blockage, by using a Caenorhabditis elegans biofilm system. Infect Immun. 2005;73:7236–42.
pubmed: 16239518
pmcid: 1273845
doi: 10.1128/IAI.73.11.7236-7242.2005
Hinnebusch BJ, Rudolph AE, Cherepanov P, Dixon JE, Schawn TG, Forsberg Å. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science. 2002;296:733–5.
pubmed: 11976454
doi: 10.1126/science.1069972
Rebeil R, Jarett CO, Driver JD, Ernst RK, Oyston PCF, Hinnebusch BJ. Induction of the Yersinia pestis PhoP-PhoQ regulatory system in the flea and its role in producing a transmissible infection. J Bacteriol. 2013;195:1920–30.
pubmed: 23435973
pmcid: 3624595
doi: 10.1128/JB.02000-12
Bobrov AG, Kirillina O, Vadyvaloo V, Koestler BJ, Hinz AK, Mack D, et al. The Yersinia pestis HmsCDE regulatory system is essential for blockage of the oriental rat flea (Xenopsylla cheopis), a classic plague vector. Environ Microbiol. 2015;17:947–59.
pubmed: 25586342
doi: 10.1111/1462-2920.12419
Eisen RJ, Gage KL. Transmission of flea-borne zoonotic agents. Annu Rev Entomol. 2012;57:61–82.
pubmed: 21888520
doi: 10.1146/annurev-ento-120710-100717
Sun Y, Connor MG, Pennington JM, Lawrenz MB. Development of bioluminescent bioreporters for in vitro and in vivo tracking of Yersinia pestis. PLoS ONE. 2012;7:e47123.
pubmed: 23071730
pmcid: 3469486
doi: 10.1371/journal.pone.0047123
Choi KH, Graynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, et al. A Tn7-based broad-range bacterial cloning and expression system. Nat Methods. 2005;2:443–8.
pubmed: 15908923
doi: 10.1038/nmeth765
Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci. 2000;97:6640–5.
pubmed: 10829079
pmcid: 18686
doi: 10.1073/pnas.120163297
Herbert AA, Guest JR. Turbidimetric and polarographic assays for lipoic acid using mutants of Escherichia coli. Methods Enzymol. 1970;18:269–72.
doi: 10.1016/0076-6879(71)18314-0
Greer 3rdLF, Szalay AA. Imaging of light emission from the expression of luciferases in living cells and organisms: a review. Luminescence. 2002;17:43–74.
pubmed: 11816060
doi: 10.1002/bio.676
Karsi A, Lawrence ML. Broad host range fluorescence and bioluminescence expression vectors for Gram-negative bacteria. Plasmid. 2007;57:286–95.
pubmed: 17207855
doi: 10.1016/j.plasmid.2006.11.002
Avci P, Karimi M, Sadasivam M, Antunes-Melo WC, Carrasco E, Hamnlin MR. In-vivo monitoring of infectious diseases in living animals using bioluminescence imaging. Virulence. 2018;9:28–63.
pubmed: 28960132
doi: 10.1080/21505594.2017.1371897
Vadyvaloo V, Viall AK, Jarett CO, Hinz AK, Sturdevant DE, Hinnebusch BJ. Role of the PhoP-PhoQ gene regulatory system in adaptation of Yersinia pestis to environmental stress in the flea digestive tract. Microbiology. 2015;161:1198–210.
pubmed: 25804213
pmcid: 4635514
doi: 10.1099/mic.0.000082
Cronan JE. Assembly of lipoic acid on its cognate enzymes: an extraordinary and essential biosynthetic pathway. Microbiol Mol Microbiol Rev. 2016;80:429–50.
doi: 10.1128/MMBR.00073-15
Douce R, Bourguignon J, Neuburger M, Rébeillé F. The glycine decarboxylase system: a fascinating complex. Trends Plant Sci. 2001;6:167–76.
pubmed: 11286922
doi: 10.1016/S1360-1385(01)01892-1
Jordan SW, Cronan JE. The Escherichia coli lipB gene encodes lipoyl (octanoyl)-acyl carrier protein:protein transferase. J Bacteriol. 2003;185:1582–9.
pubmed: 12591875
pmcid: 148080
doi: 10.1128/JB.185.5.1582-1589.2003
Reed KE, Cronan JE. Lipoic acid metabolism in Escherichia coli: sequencing and functional characterization of the lipA and lipB genes. J Bacteriol. 1993;175:1325–36.
pubmed: 8444795
pmcid: 193218
doi: 10.1128/jb.175.5.1325-1336.1993
Reed LJ, Debusk BG, Gunsalus IC, Hornberger CS. Crystalline alpha-lipoic acid; a catalytic agent associated with pyruvate dehydrogenase. Science. 1951;114:93–4.
pubmed: 14854913
doi: 10.1126/science.114.2952.93
Morris TW, Reed KE, Cronan JE. Lipoic acid metabolism in Escherichia coli: the lplA and lipB genes define redundant pathways for ligation of lipoyl groups to apoprotein. J Bacteriol. 1995;177:1–10.
pubmed: 8002607
pmcid: 176549
doi: 10.1128/jb.177.1.1-10.1995
Zhao X, Miller JR, Jiang Y, Marletta MA, Cronan JE. Assembly of the covalent linkage between lipoic acid and its cognate enzymes. Chem Biol. 2003;10:1293–302.
pubmed: 14700636
doi: 10.1016/j.chembiol.2003.11.016
Green DE, Morris TW, Green J, Cronan JE, Guest JR. Purification and properties of the lipoate protein ligase of Escherichia coli. Biochem J. 1995;309:853–62.
pubmed: 7639702
pmcid: 1135710
doi: 10.1042/bj3090853
Ali ST, Moir AJG, Ashton PR, Engel PC, Guest JR. Octanoylation of the lipoyl domains of the pyruvate dehydrogenase complex in a lipoyl-deficient strain of Escherichia coli. Mol Microbiol. 1990;4:943–50.
pubmed: 2215217
doi: 10.1111/j.1365-2958.1990.tb00667.x
Reed KE, Morris TW, Cronan JE. Mutants of Escherichia coli K-12 that are resistant to a selenium analog of lipoic acid identify unknown genes in lipoate metabolism. Proc Natl Acad Sci. 1994;91:3720–4.
pubmed: 8170976
pmcid: 43653
doi: 10.1073/pnas.91.9.3720
Morris TW, Reed KE, Cronan JE. Identification of the gene encoding lipoate-protein ligase A of Escherichia coli. Molecular cloning and characterization of the lplA gene and gene product. J Biol Chem. 1994;269:16091–100.
pubmed: 8206909
doi: 10.1016/S0021-9258(17)33977-7
Crawford MJ, Thomsen-Zieger N, Ray M, Schachtner J, Roos DS, Seeber F. Toxoplasma gondii scavenges host-derived lipoic acid despite its de novo synthesis in the apicoplast. EMBO J. 2006;25:3214–22.
pubmed: 16778769
pmcid: 1500979
doi: 10.1038/sj.emboj.7601189
Allary M, Lu JZ, Zhu L, Prigge ST. Scavenging of the cofactor lipoate is essential for the survival of the malaria parasite Plasmodium falciparum. Mol Microbiol. 2007;63:1331–44.
pubmed: 17244193
pmcid: 2796473
doi: 10.1111/j.1365-2958.2007.05592.x
Afanador GA, Guerra AJ, Swift RP, Rodriguez RE, Bartee D, Matthews KA, et al. A novel lipoate attachment enzyme is shared by Plasmodium and Chlamydia species. Mol Microbiol. 2017;106:439–51.
pubmed: 28836704
pmcid: 5653438
doi: 10.1111/mmi.13776
Vaughan JA, Azad AF. Patterns of erythrocyte digestion by bloodsucking insects: constraints on vector competence. J Med Entomol. 1993;30:214–6.
pubmed: 8094460
doi: 10.1093/jmedent/30.1.214
Flores-Mireles AL. mSphere of influence: uncovering new ways to control multidrug resistance by dissecting essential cell processes. mSphere. 2019;4:e00648–19.
pubmed: 31554727
pmcid: 6763773
doi: 10.1128/mSphere.00648-19
Goodman AL, Wu M, Gordon JI. Identifying microbial fitness determinants by insertion sequencing using genome-wide transposon mutant libraries. Nat Protoc. 2011;6:1969–80.
pubmed: 22094732
pmcid: 3310428
doi: 10.1038/nprot.2011.417
Langridge GC, Phan MD, Turner DJ, Perkins TT, Parts L, Haase J, et al. Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res. 2009;19:2308–16.
pubmed: 19826075
pmcid: 2792183
doi: 10.1101/gr.097097.109
Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 1999;285:901–6.
pubmed: 10436161
doi: 10.1126/science.285.5429.901
Zhang M, Wang C, Otto TD, Oberstaller J, Liao X, Adapa SR, et al. Uncovering the essential genes of the human malaria parasite Plasmodium falciparum by saturation mutagenesis. Science. 2018;360:eaap7847.
pubmed: 29724925
pmcid: 6360947
doi: 10.1126/science.aap7847
Van Opijnen T, Camilli A. Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms. Nat Rev Microbiol. 2013;11:435–42.
pubmed: 23712350
doi: 10.1038/nrmicro3033
Bushell E, Gomes AR, Sanderson T, Anar B, Girling G, Herd C, et al. Functional profiling of a Plasmodium Genome reveals an abundance of essential genes. Cell. 2017;170:260–72 e8.
pubmed: 28708996
pmcid: 5509546
doi: 10.1016/j.cell.2017.06.030
Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW. Simultaneous identification of bacterial virulence genes by negative selection. Science. 1995;269:400–3.
pubmed: 7618105
doi: 10.1126/science.7618105
Karlinsey JE, Stepien TA, Mayho M, Singletary LA, Bingham-Ramos LK, Brehms MA, et al. Genome-wide analysis of Salmonella enterica serovar Typhi in humanized mice reveals key virulence features. Cell Host Microbe. 2019;26:426–34.
pubmed: 31447308
pmcid: 6742556
doi: 10.1016/j.chom.2019.08.001
Phelan JP, Kern A, Ramsey ME, Lundt ME, Sharma B, Lin T, et al. Genome-wide screen identifies novel genes required for Borrelia burgdorferi survival in its Ixodes tick vector. PLoS Pathog. 2019;15:e1007644.
pubmed: 31086414
pmcid: 6516651
doi: 10.1371/journal.ppat.1007644
Jellison WL. Fleas and disease. Annu Rev Entomol. 1959;4:389–414.
doi: 10.1146/annurev.en.04.010159.002133
Truc P, Büscher P, Cuny G, Gonzatti MI, Jannin J, Joshi P, et al. Atypical human infections by animal trypanosomes. PLoS Negl Trop Dis. 2013;7:e2256.
pubmed: 24069464
pmcid: 3772015
doi: 10.1371/journal.pntd.0002256
Zhou W, Russel CW, Johnson KL, Mortensen RD, Erickson DL. Gene expression analysis of Xenopsylla cheopis (Siphonaptera: Pulicidae) suggests a role for reactive oxygen species in response to Yersinia pestis infection. J Med Entomol. 2012;49:364–70.
pubmed: 22493856
doi: 10.1603/ME11172
Bontemps-Gallo S, Lawrence K, Gherardini FC. Two different virulence-related regulatory pathways in Borrelia burgdorferi are directly affected by osmotic fluxes in the blood meal of feeding ixodes ticks. PLoS Pathog. 2016;12:e1005791.
pubmed: 27525653
pmcid: 4985143
doi: 10.1371/journal.ppat.1005791
Vallet-Gely I, Lemaitre B, Boccard F. Bacterial strategies to overcome insect defences. Nat Rev Microbiol. 2008;6:302–13.
pubmed: 18327270
doi: 10.1038/nrmicro1870
Melo RFP, Guarneri AA, Silber AM. The influence of environmental cues on the development of Trypanosoma cruzi in triatominae vector. Front Cell Infect Microbiol. 2020;10:27.
pubmed: 32154185
pmcid: 7046586
doi: 10.3389/fcimb.2020.00027
Vodovar N, Vinals M, Liehl P, Basset A, Degrouard J, Spellman P, et al. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci. 2005;102:11414–19.
pubmed: 16061818
pmcid: 1183552
doi: 10.1073/pnas.0502240102
Booker SJ. Unraveling the pathway of lipoic acid biosynthesis. Chem Biol. 2004;11:10–2.
pubmed: 15112987
doi: 10.1016/j.chembiol.2004.01.002
Herbert AA, Guest JR. Biochemical and genetic studies with lysine+methionine mutants of Escherichia coli: lipoic acid and alpha-ketoglutarate dehydrogenase-less mutants. J Gen Microbiol. 1968;53:363–81.
pubmed: 4889470
doi: 10.1099/00221287-53-3-363
Vanden Boom TJ, Reed KE, Cronan JE. Lipoic acid metabolism in Escherichia coli: isolation of null mutants defective in lipoic acid biosynthesis, molecular cloning and characterization of the E. coli lip locus, and identification of the lipoylated protein of the glycine cleavage system. J Bacteriol. 1991;173:6411–20.
pubmed: 1655709
pmcid: 208974
doi: 10.1128/jb.173.20.6411-6420.1991
Zhao X, Miller JR, Cronan JE. The reaction of LipB, the octanoyl-[acyl carrier protein]:protein N-octanoyltransferase of lipoic acid synthesis, proceeds through an acyl-enzyme intermediate. Biochemistry. 2005;44:16737–46.
pubmed: 16342964
doi: 10.1021/bi051865y
Miller JR, Busby RW, Jordan SW, Cheek J, Henshaw TF, Ashley GW, et al. Escherichia coli LipA is a lipoyl synthase: in vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoyl-acyl carrier protein. Biochemistry. 2000;39:15166–78.
pubmed: 11106496
doi: 10.1021/bi002060n
Laczkovich I, Teoh WP, Flury S, Grayczyk JP, Zorzoli A, Alonzo 3rd F. Increased flexibility in the use of exogenous lipoic acid by Staphylococcus aureus. Mol Microbiol. 2018;109:150–68.
doi: 10.1111/mmi.13970
Spalding MD, Prigge ST. Lipoic acid metabolism in microbial pathogens. Microbiol Mol Biol Rev. 2010;74:200–28.
pubmed: 20508247
pmcid: 2884412
doi: 10.1128/MMBR.00008-10
Pain A, Renauld H, Berriman M, Murphy L, Yeats CA, Weir W, et al. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science. 2005;309:131–3.
pubmed: 15994557
doi: 10.1126/science.1110418
Keeney K, Colosi L, Weber W, O’Riordan M. Generation of branched-chain fatty acids through lipoate dependent metabolism facilitates intracellular growth of Listeria monocytogenes. J Bacteriol. 2009;191:2187–96.
pubmed: 19181817
pmcid: 2655518
doi: 10.1128/JB.01179-08
O’Riordan M, Moors MA, Portnoy DA. Listeria intracellular growth and virulence require host-derived lipoic acid. Science. 2003;302:462–4.
pubmed: 14564012
doi: 10.1126/science.1088170
Grayczyk JP, Harvey CJ, Laczkovich I, Alonzo 3rdF. A lipoylated metabolic protein released by Staphylococcus aureus suppresses macrophage activation. Cell Host Microbe. 2017;22:678–87.
pubmed: 29056428
pmcid: 5683407
doi: 10.1016/j.chom.2017.09.004
Zorzoli A, Grayczyk JP, Alonzo 3rdF. Staphylococcus aureus tissue infection during sepsis is supported by differential use of bacterial or host-derived lipoic acid. PLoS Pathog. 2016;12:e1005933.
pubmed: 27701474
pmcid: 5049849
doi: 10.1371/journal.ppat.1005933