Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12 View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2006-10-06

AUTHORS

Everett T Hayes, Jessica C Wilks, Piero Sanfilippo, Elizabeth Yohannes, Daniel P Tate, Brian D Jones, Michael D Radmacher, Sandra S BonDurant, Joan L Slonczewski

ABSTRACT

BackgroundIn Escherichia coli, pH regulates genes for amino-acid and sugar catabolism, electron transport, oxidative stress, periplasmic and envelope proteins. Many pH-dependent genes are co-regulated by anaerobiosis, but the overall intersection of pH stress and oxygen limitation has not been investigated.ResultsThe pH dependence of gene expression was analyzed in oxygen-limited cultures of E. coli K-12 strain W3110. E. coli K-12 strain W3110 was cultured in closed tubes containing LBK broth buffered at pH 5.7, pH 7.0, and pH 8.5. Affymetrix array hybridization revealed pH-dependent expression of 1,384 genes and 610 intergenic regions. A core group of 251 genes showed pH responses similar to those in a previous study of cultures grown with aeration. The highly acid-induced gene yagU was shown to be required for extreme-acid resistance (survival at pH 2). Acid also up-regulated fimbriae (fimAC), periplasmic chaperones (hdeAB), cyclopropane fatty acid synthase (cfa), and the "constitutive" Na+/H+ antiporter (nhaB). Base up-regulated core genes for maltodextrin transport (lamB, mal), ATP synthase (atp), and DNA repair (recA, mutL). Other genes showed opposite pH responses with or without aeration, for example ETS components (cyo,nuo, sdh) and hydrogenases (hya, hyb, hyc, hyf, hyp). A hypF strain lacking all hydrogenase activity showed loss of extreme-acid resistance. Under oxygen limitation only, acid down-regulated ribosome synthesis (rpl,rpm, rps). Acid up-regulated the catabolism of sugar derivatives whose fermentation minimized acid production (gnd, gnt, srl), and also a cluster of 13 genes in the gadA region. Acid up-regulated drug transporters (mdtEF, mdtL), but down-regulated penicillin-binding proteins (dacACD, mreBC). Intergenic regions containing regulatory sRNAs were up-regulated by acid (ryeA, csrB, gadY, rybC).ConclusionpH regulates a core set of genes independently of oxygen, including yagU, fimbriae, periplasmic chaperones, and nhaB. Under oxygen limitation, however, pH regulation is reversed for genes encoding electron transport components and hydrogenases. Extreme-acid resistance requires yagU and hydrogenase production. Ribosome synthesis is down-regulated at low pH under oxygen limitation, possibly due to the restricted energy yield of catabolism. Under oxygen limitation, pH regulates metabolism and transport so as to maximize alternative catabolic options while minimizing acidification or alkalinization of the cytoplasm. More... »

PAGES

89

Identifiers

URI

http://scigraph.springernature.com/pub.10.1186/1471-2180-6-89

DOI

http://dx.doi.org/10.1186/1471-2180-6-89

DIMENSIONS

https://app.dimensions.ai/details/publication/pub.1016974365

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/17026754


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43 activity
44 aeration
45 alkalinization
46 anaerobiosis
47 antiporter
48 array hybridization
49 broth
50 catabolism
51 chaperones
52 closed tube
53 clusters
54 coli
55 coli K
56 components
57 composition
58 core genes
59 core group
60 core set
61 culture
62 cyclopropane fatty acid synthase
63 cytoplasm
64 dependence
65 derivatives
66 drug transporters
67 electron transport
68 electron transport components
69 energy yield
70 envelope protein
71 expression
72 extreme acid resistance
73 fatty acid synthase
74 fimbriae
75 gene expression
76 genes
77 group
78 hybridization
79 hydrogenase activity
80 hydrogenases
81 intergenic region
82 intersection
83 limitations
84 loss
85 low pH
86 maltodextrin transport
87 metabolism
88 multidrug transporter
89 options
90 overall intersection
91 oxidative stress
92 oxygen
93 oxygen limitation
94 oxygen-limited cultures
95 pH
96 pH regulation
97 pH-dependent expression
98 penicillin-binding proteins
99 periplasmic chaperone
100 previous studies
101 production
102 protein
103 region
104 regulation
105 regulation of catabolism
106 regulatory sRNAs
107 repair
108 resistance
109 response
110 ribosome synthesis
111 sRNAs
112 set
113 strain W3110
114 strains
115 stress
116 study
117 sugar catabolism
118 sugar derivatives
119 synthase
120 synthesis
121 transport
122 transport components
123 transporters
124 tube
125 yield
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