Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria
Bacteria in various habitats are subject to continuously changing environmental conditions, such as nutrient deprivation, heat and cold stress, UV radiation, oxidative stress, dessication, acid stress, nitrosative stress, cell envelope stress, heavy metal exposure, osmotic stress, and others. In order to survive, they have to respond to these conditions by adapting their physiology through sometimes drastic changes in gene expression. In addition they may adapt by changing their morphology, forming biofilms, fruiting bodies or spores, filaments, Viable But Not Culturable (VBNC) cells or moving away from stress compounds via chemotaxis. Changes in gene expression constitute the main component of the bacterial response to stress and environmental changes, and involve a myriad of different mechanisms, including (alternative) sigma factors, bi- or tri-component regulatory systems, small non-coding RNA’s, chaperones, CHRIS-Cas systems, DNA repair, toxin-antitoxin systems, the stringent response, efflux pumps, alarmones, and modulation of the cell envelope or membranes, to name a few. Many regulatory elements are conserved in different bacteria; however there are endless variations on the theme and novel elements of gene regulation in bacteria inhabiting particular environments are constantly being discovered. Especially in (pathogenic) bacteria colonizing the human body a plethora of bacterial responses to innate stresses such as pH, reactive nitrogen and oxygen species and antibiotic stress are being described. An attempt is made to not only cover model systems but give a broad overview of the stress-responsive regulatory systems in a variety of bacteria, including medically important bacteria, where elucidation of certain aspects of these systems could lead to treatment strategies of the pathogens. Many of the regulatory systems being uncovered are specific, but there is also considerable “cross-talk” between different circuits. Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria is a comprehensive two-volume work bringing together both review and original research articles on key topics in stress and environmental control of gene expression in bacteria. Volume One contains key overview chapters, as well as content on one/two/three component regulatory systems and stress responses, sigma factors and stress responses, small non-coding RNAs and stress responses, toxin-antitoxin systems and stress responses, stringent response to stress, responses to UV irradiation, SOS and double stranded systems repair systems and stress, adaptation to both oxidative and osmotic stress, and desiccation tolerance and drought stress. Volume Two covers heat shock responses, chaperonins and stress, cold shock responses, adaptation to acid stress, nitrosative stress, and envelope stress, as well as iron homeostasis, metal resistance, quorum sensing, chemotaxis and biofilm formation, and viable but not culturable (VBNC) cells.Covering the full breadth of current stress and environmental control of gene expression studies and expanding it towards future advances in the field, these two volumes are a one-stop reference for (non) medical molecular geneticists interested in gene regulation under stress.
VOLUME 1 Preface, xiii Acknowledgements, xiv List of contributors, xv 1 Introduction, 1Frans J. de Bruijn Section 2: Key overview chapters, 3 2.1 Stress-induced changes in transcript stability, 5Dvora Biran and Eliora Z. Ron 2.2 StressChip for monitoring microbial stress response in the environment, 9Joy D. Van Nostrand, Aifen Zhou and Jizhong Zhou 2.3 A revolutionary paradigm of bacterial genome regulation, 23Akira Ishihama 2.4 Role of changes in ?70-driven transcription in adaptation of E. coli to conditions of stress or starvation, 37Umender K. Sharma 2.5 The distribution and spatial organization of RNA polymerase in Escherichia coli: growth rate regulation and stress responses, 48Ding Jun Jin, Cedric Cagliero, Jerome Izard, Carmen Mata Martin, and Yan Ning Zhou 2.6 The ECF classification: a phylogenetic reflection of the regulatory diversity in the extracytoplasmic function ? factor protein family, 64Daniela Pinto andThorsten Mascher 2.7 Toxin–antitoxin systems in bacteria and archaea, 97Yoshihiro Yamaguchi and Masayori Inouye 2.8 Bacterial sRNAs: regulation in stress, 108Marimuthu Citartan, Carsten A. Raabe, Chee-Hock Hoe, Timofey S. Rozhdestvensky, andThean-Hock Tang 2.9 Bacterial stress responses as determinants of antimicrobial resistance, 115Michael Fruci and Keith Poole 2.10 Transposable elements: a toolkit for stress and environmental adaptation in bacteria, 137Anna Ullastres, Miriam Merenciano, Lain Guio, and Josefa González 2.11 CRISPR–Cas system: a new paradigm for bacterial stress response through genome rearrangement, 146Joseph A. Hakim, Hyunmin Koo, Jan D. van Elsas, Jack T. Trevors, and Asim K. Bej 2.12 The copper metallome in prokaryotic cells, 161Christopher Rensing, Hend A. Alwathnani, and Sylvia F. McDevitt 2.13 Ribonucleases as modulators of bacterial stress response, 174Cátia Bárria, Vánia Pobre, Afonso M. Bravo, and Cecília M. Arraiano 2.14 Double-strand-break repair, mutagenesis, and stress, 185Elizabeth Rogers, Raul Correa, Brittany Barreto, María Angélica Bravo Núñez, P.J. Minnick, Diana Vera Cruz, Jun Xia, P.J. Hastings, and Susan M. Rosenberg 2.15 Sigma factor competition in Escherichia coli: kinetic and thermodynamic perspectives, 196Kuldeepkumar Ramnaresh Gupta and Dipankar Chatterji 2.16 Iron homeostasis and iron–sulfur cluster assembly in Escherichia coli, 203Huangen Ding 2.17 Mechanisms underlying the antimicrobial capacity of metals, 215Joe A. Lemire and Raymond J. Turner 2.18 Acyl-homoserine lactone-based quorum sensing in members of the marine bacterial Roseobacter clade: complex cell-to-cell communication controls multiple physiologies, 225Alison Buchan, April Mitchell,W. Nathan Cude, and Shawn Campagna 2.19 Native and synthetic gene regulation to nitrogen limitation stress, 234J örg Schumacher Section 3: One-, two-, and three-component regulatory systems and stress responses, 247 3.1 Two-component systems that control the expression of aromatic hydrocarbon degradation pathways, 249\Tino Krell 3.2 Cross-talk of global regulators in Streptomyces, 257Juan F. Martín, Fernando Santos-Beneit, Alberto Sola-Landa, and Paloma Liras 3.3 NO–H-NOX-regulated two-component signaling, 268Dhruv P. Arora, Sandhya Muralidharan, and Elizabeth M. Boon 3.4 The two-component CheY system in the chemotaxis of Sinorhizobium meliloti, 277Martin Haslbeck 3.5 Stimulus perception by histidine kinases, 282Hannah Schramke, Yang Wang, Ralf Heermann, and Kirsten Jung Section 4: Sigma factors and stress responses, 301 4.1 The extracytoplasmic function sigma factor EcfO protects Bacteroides fragilis against oxidative stress, 303Ivan C. Ndamukong, Samantha Palethorpe, Michael Betteken, and C. Jeffrey Smith 4.2 Regulation of energy metabolism by the extracytoplasmic function (ECF) ? factors of Arcobacter butzleri, 311Irati Martinez-Malaxetxebarria, Rudy Muts, Linda van Dijk, Craig T. Parker, William G. Miller, Steven Huynh,Wim Gaastra, Jos P.M. van Putten, Aurora Fernandez-Astorga, and Marc M.S.M Wösten 4.3 Extracytoplasmic function sigma factors and stress responses in Corynebacterium pseudotuberculosis, 321Thiago L.P. Castro, Nubia Seyffert, Anne C. Pinto, Artur Silva, Vasco Azevedo, and Luis G.C. Pacheco 4.4 The complex roles and regulation of stress response ? factors in Streptomyces coelicolor, 328Jan Kormanec, Beatrica Sevcikova, Renata Novakova, Dagmar Homerova, Bronislava Rezuchova, and Erik Mingyar 4.5 Proteolytic activation of extra cytoplasmic function (ECF) ? factors, 344JessicaL. Hastie and Craig D. Ellermeier 4.6 The ECF family sigma factor ?H in Corynebacterium glutamicum controls the thiol-oxidative stress response, 352Tobias Busche and Jörn Kalinowski 4.7 Posttranslational regulation of antisigma factors of RpoE: a comparison between the Escherichia coli and Pseudomonas aeruginosa systems, 361Sundar Pandey, Kyle L. Martins, and Kalai Mathee Section 5: Small noncoding RNAs and stress responses, 369 5.1 Bacterial small RNAs in mixed regulatory circuits, 371Jonathan Jagodnik, DenisThieffry, and Maude Guillier 5.2 Role of small RNAs in Pseudomonas aeruginosa virulence and adaptation, 383Hansi Kumari, Deepak Balasubramanian, and Kalai Mathee 5.3 Physiological effects of posttranscriptional regulation by the small RNA SgrS during metabolic stress inEscherichia coli, 393Gregory R. Richards 5.4 Three rpoS-activating small RNAs in pathways contributing to acid resistance of Escherichia coli, 402Geunu Bak, Kook Han, Daun Kim, Kwang-sun Kim, and Younghoon Lee 5.5 Thermal stress noncoding RNAs in prokaryotes and eukaryotes: a comparative approach, 412Mercedes de la Fuente and José Luis Martínez-Guitarte Section 6: Toxin-antitoxin systems and stress responses, 423 6.1 Epigenetics mediated by restriction modification systems, 425Iwona Mruk and Ichizo Kobayashi 6.2 Toxin–antitoxin systems as regulators of bacterial fitness and virulence, 437Brittany A. Fleming and Matthew A. Mulvey 6.3 Mechanisms of stress-activated persister formation in Escherichia coli, 446Stephanie M. Amato and Mark P. Brynildsen 6.4 Identification and characterization of type II toxin–antitoxin systems in the opportunistic pathogenAcinetobacter baumannii, 454Edita Sûziedéliené, Milda Jurénaité, and Julija Armalyté 6.5 Transcriptional control of toxin–antitoxin expression: keeping toxins under wraps until the time is right, 463Barbara K?edzierska and Finbarr Hayes 6.6 Opposite effects of GraT toxin on stress tolerance of Pseudomonas putida, 473Rita Hõrak and Hedvig Tamman Section 7: Stringent response to stress, 479 7.1 Preferential cellular accumulation of ppGpp or pppGpp in Escherichia coli, 481K. Potrykus and M. Cashel 7.2 Global Rsh-dependent transcription profile of Brucella suis during stringent response unravels adaptation to nutrient starvation and cross-talk with other stress responses, 489Stephan Köhler, Nabil Hanna, Safia Ouahrani-Bettache, Kenneth L. Drake, L. Garry Adams, and Alessandra Occhialini 7.3 The stringent response and antioxidant defences in Pseudomonas aeruginosa, 500Gowthami Sampathkumar, Malika Khakimova, Tevy Chan, and Dao Nguyen 7.4 Molecular basis of the stringent response in Vibrio cholerae, 507Shreya Dasgupta, Bhabatosh Das, Pallabi Basu, and Rupak K. Bhadra Section 8: Responses to UV irradiation, 517 8.1 UV stress-responsive genes associated with ICE SXT/R391 group, 519Patricia Armshaw and J. Tony Pembroke 8.2 Altered outer membrane proteins in response to UVC radiation in Vibrio parahaemolyticus and Vibrio alginolyticus, 528Fethi Ben Abdallah 8.3 Ultraviolet-B radiation effects on the community, physiology, and mineralization of magnetotactic bacteria, 532Yingzhao Wang and Yongxin Pan 8.4 Nucleotide excision repair system and gene expression in Mycobacterium smegmatis, 545Angelina Cordone Section 9: SOS and double stranded repair systems and stress, 551 9.1 The SOS response modulates bacterial pathogenesis, 553Darja ??Zgur Bertok 9.2 RNAP secondary-channel interactors in Escherichia coli: makers and breakers of genome stability, 561Priya Sivaramakrishnan and Christophe Herman 9.3 How a large gene network couples mutagenic DNA break repair to stress in Escherichia coli, 570Elizabeth Rogers, P.J. Hastings, María Angélica Bravo Núñez, and Susan M. Rosenberg 9.4 Double-strand DNA break repair in mycobacteria, 577Richa Gupta and Michael S. Glickman Section 10: Adaptation to oxidative stress, 587 10.1 Peroxide-sensing transcriptional regulators in bacteria, 58James M. Dubbs and Skorn Mongkolsuk 10.2 Regulation of oxidative stress–related genes implicated in the establishment of opportunistic infections by Bacteroides fragilis, 603Felipe Lopes Teixeira, Regina Maria Cavalcanti Pilotto Domingues, and Leandro Araujo Lobo 10.3 Investigation into oxidative stress response of Shewanella oneidensis reveals a distinct mechanism, 609Jie Yuan, Fen Wan, and Haichun Gao 10.4 An omics view on the response to singlet oxygen, 619Bork A. Berghoff and Gabriele Klug 10.5 Regulators of oxidative stress response genes in Escherichia coli and their conservation in bacteria, 632Herb E. Schellhorn, Mohammad Mohiuddin, Sarah M. Hammond, and Steven Botts 10.6 Hydrogen peroxide resistance in Bifidobacterium animalis subsp. lactis and Bifidobacterium longum, 638Taylor S. Oberg and Jeff R. Broadbent Section 11: Adaptation to osmotic stress, 647 11.1 Interstrain variation in the physiological and transcriptional responses of Pseudomonas syringae to osmotic stress, 649Gwyn A. Beattie, Chiliang Chen, Lindsey Nielsen, and Brian C. Freeman 11.2 Management of osmotic stress by Bacillus subtilis: genetics and physiology, 657Tamara Hoffmann and Erhard Bremer 11.3 Hyperosmotic response of Streptococcus mutans: from microscopic physiology to transcriptomic profile, 677Lu Wang and Xin Xu 11.4 Defective ribosome maturation or function makes Escherichia coli cells salt-resistant, 687Hyouta Himeno, Takefusa Tarusawa, Shion Ito, and Simon Goto Section 12: Dessication tolerance and drought stress, 693 12.1 Consequences of elevated salt concentrations on expression profiles in the rhizobium S. meliloti 1021 likely involved in heat and desiccation stress, 695Jan A.C. Vriezen, Caroline M. Finn, and Klaus Nüsslein 12.2 Genes involved in the formation of desiccationresistant cysts in Azotobacter vinelandii, 709Guadalupe Espín 12.3 Osmotic and desiccation tolerance in Escherichia coli O157:H7 and Salmonella enterica requires rpoS (?38), 716Zach Pratt, Megan Shiroda, Andrew J. Stasic, Josh Lensmire, and C.W. Kaspar 12.4 Desiccation of Salmonella enterica induces cross-tolerance to other stresses, 725Shlomo Sela (Saldinger) and Chellaiah Edward Raja Index, i1 VOLUME 2 Preface, xiii Acknowledgements, xiv List of contributors, xv Section 13: Heat shock responses, 737 13.1 Heat shock response in bacteria with large genomes: lessons from rhizobia, 739Ana Alexandre and Solange Oliveira 13.2 Small heat shock proteins in bacteria, 747Martin Haslbeck 13.3 Transcriptome analysis of bacterial response to heat shock using next-generation sequencing, 754Kok-Gan Chan 13.4 Comparative analyses of bacterial transcriptome reorganisation in response to temperature increase, 757Bei-Wen Ying and Tetsuya Yomo 13.5 Participation of Ser–Thr protein kinases in regulation of heat stress responses in Synechocystis, 766Anna A. Zorina, Galina V. Novikova, and Dmitry A. Los Section 14: Chaperonins and stress, 781 14.1 GroEL/ES chaperonin: unfolding and refolding reactions, 783Victor V. Marchenkov, Nataliya A. Ryabova, Olga M. Selivanova, and Gennady V. Semisotnov 14.2 Functional comparison between the DnaK chaperone systems of Streptococcus intermedius and Escherichia coli, 791Toshifumi Tomoyasu and Hideaki Nagamune 14.3 Coevolution analysis illuminates the evolutionary plasticity of the chaperonin system GroES/L, 796Mario A. Fares 14.4 ClpL ATPase: a novel chaperone in bacterial stress responses, 812Pratick Khara and Indranil Biswas 14.5 Duplicated groEL genes inMyxococcus xanthus DK1622, 820Yan Wang, Xiao-jing Chen, and Yue-zhong Li Section 15: Cold shock responses, 827 15.1 Gene regulation by cold shock proteins via transcription antitermination, 829Sangita Phadtare and Konstantin Severinov 15.2 Metagenomic analysis of microbial cold stress proteins in polar lacustrine ecosystems, 837Hyunmin Koo, Joseph A. Hakim, and Asim K. Bej 15.3 Role of two-component systems in cold tolerance of Clostridium botulinum, 845Yâgmur Derman, Elias Dahlsten, and Hannu Korkeala 15.4 Cold shock CspA protein production during periodic temperature cycling in Escherichia coli, 854David Stopar and Tina Ivancic 15.5 Cold shock response in Escherichia coli: a model system to study posttranscriptional regulation, 859Anna Maria Giuliodori 15.6 New insight into cold shock proteins: RNA-binding proteins involved in stress response and virulence, 873Charlotte Michaux and Jean-Christophe Giard 15.7 Light regulation of cold stress responses in Synechocystis, 881Kirill S. Mironov and Dmitry A. Los 15.8 Escherichia coli cold shock gene profiles in response to overexpression or deletion of CsdA, RNase R, andPNPase and relevance to low-temperature RNA metabolism, 890Sangita Phadtare Section 16: Adaptation to acid stress, 897 16.1 Acid-adaptive responses of Streptococcus mutans, and mechanisms of integration with oxidative stress, 899Robert G. Quivey Jr., Roberta C. Faustoferri, Brendaliz Santiago, Jonathon Baker, Benjamin Cross, and Jin Xiao 16.2 Acid survival mechanisms in neutralophilic bacteria, 911Eugenia Pennacchietti, Fabio Giovannercole, and Daniela De Biase 16.3 Two-component systems in sensing and adapting to acid stress in Escherichia coli, 927Yoko Eguchi and Ryutaro Utsumi 16.4 Slr1909, a novel two-component response regulator involved in acid tolerance in Synechocystis sp. PCC 6803, 935Lei Chen, Qiang Ren, Jiangxin Wang, and Weiwen Zhang 16.5 Comparative mass spectrometry–based proteomics to elucidate the acid stress response in Lactobacillusplantarum, 944Tiaan Heunis, Shelly Deane, and Leon M.T. Dicks Section 17: Adaptation to nitrosative stress, 95317.1 Transcriptional regulation by thiol-based sensors of oxidative and nitrosative stress, 955Timothy Tapscott, Matthew A. Crawford, and Andr´es Vázquez-Torres 17.2 Haemoglobins of Mycobacterium tuberculosis and their involvement in management of environmental stress, 967Kanak L. Dikshit 17.3 What is it about NO that you don’t understand? The role of heme and HcpR in Porphyromonas gingivalis’s response to nitrate (NO3), nitrite (NO2), and nitric oxide (NO), 976Janina P. Lewis and Benjamin R. Belvin 17.4 Di-iron RICs: players in nitrosative-oxidative stress defences, 989Lígia S. Nobre and Lí?Ygia M. Saraiva 17.5 The Vibrio cholerae stress response: an elaborate system geared toward overcoming host defenses during infection, 997Karl-Gustav Rueggeberg and Jun Zhu 17.6 Ensemble modeling enables quantitative exploration of bacterial nitric oxide stress networks, 1009Jonathan L. Robinson and Mark P. Brynildsen Section 18: Adaptation to cell envelope stress, 1015 18.1 The Cpx inner membrane stress response, 1017Randi L. Guest and Tracy L. Raivio 18.2 New insights into stimulus detection and signal propagation by the Cpx-envelope stress system, 1025Patrick Hoernschemeyer and Sabine Hunke 18.3 Promiscuous functions of cell envelope stress-sensing systems in Klebsiella pneumoniae and Acinetobacterbaumannii, 1031Vijaya Bharathi Srinivasan and Govindan Rajamohan 18.4 Influence of BrpA and Psr on cell envelope homeostasis and virulence of Streptococcus mutans, 1043Zezhang T.Wen, Jacob P. Bitoun, Sumei Liao, and Jacqueline Abranches 18.5 Modulators of the bacterial two-component systems involved in envelope stress, transport, and virulence, 1055Rajeev Misra Section 19: Iron homeostasis, 1065 19.1 Iron homeostasis and environmental responses in cyanobacteria: regulatory networks involving Fur, 1067María Luisa Peleato, María Teresa Bes, and María F. Fillat 19.2 Interplay between O2 and iron in gene expression: environmental sensing by FNR, ArcA, and Fur in bacteria, 1079Bryan Troxell and Hosni M. Hassan 19.3 The iron–sulfur cluster biosynthesis regulator IscR contributes to iron homeostasis and resistance tooxidants in Pseudomonas aeruginosa, 1090Adisak Romsang, James M. Dubbs, and Skorn Mongkolsuk 19.4 Transcriptional analysis of iron-responsive regulatory networks in Caulobacter crescentus, 1103José F. da Silva Neto 19.5 Protein–protein interactions regulate the release of iron stored in bacterioferritin, 1109Huili Yao, YanWang, and Mario Rivera 19.6 Protein dynamics and ion traffic in bacterioferritin function: a molecular dynamics simulation study onwild-type and mutant Pseudomonas aeruginosa BfrB, 1118Huan Rui, Mario Rivera, and Wonpil Im Section 20: Metal resistance, 1131 20.1 Nickel toxicity, regulation, and resistance in bacteria, 1133Lee Macomber and Robert P. Hausinger 20.2 Metabolic networks to counter Al toxicity in Pseudomonas fluorescens: a holistic view, 1145Christopher Auger, Nishma D. Appanna, and Vasu D. Appanna 20.3 Genomics of the resistance to metal and oxidative stresses in cyanobacteria, 1154Corinne Cassier-Chauvat and Franck Chauvat 20.4 Cross-species transcriptional network analysis reveals conservation and variation in response to metal stress in cyanobacteria, 1165Jiangxin Wang, Gang Wu, Lei Chen, and Weiwen Zhang 20.5 The extracytoplasmic function sigma factor–mediated response to heavy metal stress in Caulobacter crescentus, 1171Rogério F. Lourenco and Suely L. Gomes 20.6 Metal ion toxicity and oxidative stress in Streptococcus pneumoniae, 1184Christopher A. McDevitt, Stephanie L. Begg, and James C. Paton Section 21: Quorum sensing, 1195 21.1 Quorum sensing and bacterial social interactions in biofilms: bacterial cooperation and competition, 1197Yung-Hua Li and Xiao-Lin Tian 21.2 Recent advances in bacterial quorum quenching, 1206Kok-Gan Chan, Wai-Fong Yin, and Kar-Wai Hong 21.3 LuxR-type quorum-sensing regulators that are antagonized by cognate pheromones, 1221Stephen C. Winans, Ching-Sung Tsai, Gina T. Ryan, Ana Lidia Flores-Mireles, Esther Costa, Kevin Y. Shih, Thomas C.Winans, Youngchang Kim, Robert Jedrzejczak, and Gekleng Chhor 21.4 Adaptation to environmental stresses in Streptococcus mutans through the production of its quorum-sensing peptide pheromone, 1232Delphine Dufour, Vincent Leung, and Céline M. Lévesque 21.5 Quorum sensing in Bacillus cereus in relation to cysteine metabolism and the oxidative stress response, 1242Eugénie Huillet and Michel Gohar Section 22: Chemotaxis and biofilm formation, 1253 22.1 The flagellum as a sensor, 1255Rasika M. Harshey 22.2 Flagellar motility and fitness in xanthomonads, 1265Marie-Agnès Jacques, Jean-Françis Guimbaud, Martial Briand, Arnaud Indiana, and Armelle Darrasse 22.3 Understanding Listeriamonocytogenes biofilms: perspectives into mechanisms of adaptation and regulation under stress conditions, 1274Lizziane Kretli Winkelströter, Fernanda Barbosa dos Reis-Teixeira, Gabriela Satti Lameu, and Elaine Cristina Pereira De Martinis 22.4 Biofilm formation and environmental signals in Bordetella, 1279Tomoko Hanawa 22.5 Biofilm formation by rhizobacteria in response to water-limiting conditions, 1287Pablo Bogino, Fiorela Nievas, and Walter Giordano 22.6 Stress conditions triggering mucoid-to-nonmucoid morphotype variation in Burkholderia, and effects onvirulence and biofilm formation, 1295Leonilde M. Moreira, Inês N. Silva, Ana S. Ferreira, and Mário R. Santos 22.7 Effect of environmental conditions present in the fishery industry on the biofilm-forming ability of Staphylococcus aureus, 1304Daniel Vázquez-Sánchez 22.8 Biofilm development and stress response in the cholera bacterium, 1310Anisia J. Silva and Jorge A. Benitez 22.9 Outer membrane vesicle secretion: from envelope stress to biofilm formation, 1322Thomas Baumgarten and Hermann J. Heipieper Section 23: Viable but nonculturable (VBNC) cells, 1329 23.1 Resuscitation of Vibrios fromthe viable but nonculturable state is induced by quorum-sensing molecules, 1331Mesrop Ayrapetyan, Tiffany C. Williams, and James D. Oliver 23.2 Differential resuscitative effects of pyruvate and its analogs on VBNC (viable but nonculturable)Salmonella, 1338Fumio Amano 23.3 Environmental persistence of Shiga toxin–producing E. coli, 1346Philipp Aurass and Antje Flieger 23.4 Of a tenacious and versatile relic: the role of inorganic polyphosphate (poly-P) metabolism in the survival, adaptation, and virulence of Campylobacter jejuni, 1354Issmat I. Kassem and Gireesh Rajashekara Index, i1
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