Polyamines Stimulate the Level of the σ38 Subunit (RpoS) of Escherichia coli RNA Polymerase, Resulting in the Induction of the Glutamate Decarboxylase-dependent Acid Response System via the gadE Regulon

Chattopadhyay, Manas K.; Keembiyehetty, Chithra N.; Chen, Weiping; Tabor, Herbert

doi:10.1074/jbc.m115.655688

Cited by 25 publications

(30 citation statements)

References 59 publications

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“…promoter region, which is known to be highly RpoS dependent and has been used by others as reporter of RpoS activity (57)(58)(59). A microscopic analysis of stationary-phase cultures grown at 37°C revealed that all strains showed significant GFP expression, with the exception of the BW25113⌬rpoS mutant strain, which showed no detectable fluorescence.…”

Section: Resultsmentioning

confidence: 99%

The General Stress Response Is Conserved in Long-Term Soil-Persistent Strains of Escherichia coli

Somorin

Abram

Brennan

et al. 2016

Appl Environ Microbiol

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Although Escherichia coli is generally considered to be predominantly a commensal of the gastrointestinal tract, a number of recent studies suggest that it is also capable of long-term survival and growth in environments outside the host. As the extraintestinal physical and chemical conditions are often different from those within the host, it is possible that distinct genetic adaptations may be required to enable this transition. Several studies have shown a trade-off between growth and stress resistance in nutrient-poor environments, with lesions in the rpoS locus, which encodes the stress sigma factor RpoS ( S ). In this study, we investigated a unique collection of long-term soil-persistent E. coli isolates to determine whether the RpoS-controlled general stress response is altered during adaptation to a nutrient-poor extraintestinal environment. The sequence of the rpoS locus was found to be highly conserved in these isolates, and no nonsense or frameshift mutations were detected. Known RpoS-dependent phenotypes, including glycogen synthesis and ␥-aminobutyrate production, were found to be conserved in all strains. All strains expressed the full-length RpoS protein, which was fully functional using the RpoS-dependent promoter reporter fusion PgadX:: gfp. RpoS was shown to be essential for long-term soil survival of E. coli, since mutants lacking rpoS lost viability rapidly in soil survival assays. Thus, despite some phenotypic heterogeneity, the soil-persistent strains all retained a fully functional RpoS-regulated general stress response, which we interpret to indicate that the stresses encountered in soil provide a strong selective pressure for maintaining stress resistance, despite limited nutrient availability. IMPORTANCEEscherichia coli has been, and continues to be, used as an important indicator species reflecting potential fecal contamination events in the environment. However, recent studies have questioned the validity of this, since E. coli has been found to be capable of long-term colonization of soils. This study investigated whether long-term soil-persistent E. coli strains have evolved altered stress resistance characteristics. In particular, the study investigated whether the main regulator of genes involved in stress protection, the sigma factor RpoS, has been altered in the soil-persistent strains. The results show that RpoS stress protection is fully conserved in soil-persistent strains of E. coli. They also show that loss of the rpoS gene dramatically reduces the ability of this organism to survive in a soil environment. Overall, the results indicate that soil represents a stressful environment for E. coli, and their survival in it requires that they deploy a full stress protection response. E scherichia coli is a Gram-negative, facultative anaerobe, belonging to the Enterobacteriaceae family, which inhabits the intestinal tracts of humans, warm-blooded animals, and reptiles (1, 2). It can be transferred through water and sediments via feces and is almost universally used as an i...

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Section: Resultsmentioning

confidence: 99%

The General Stress Response Is Conserved in Long-Term Soil-Persistent Strains of Escherichia coli

Somorin

Abram

Brennan

et al. 2016

Appl Environ Microbiol

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“…Polyamines stimulate synthesis of specific proteins in E. coli cells through mRNA transcription and stabilizing various RNA‐RNA interactions (Chattopadhyay et al . ; Igarashi & Kashiwagi ). It is possible that some long and branched polyamines are involved in regulating the expression of certain proteins.…”

Section: Discussionmentioning

confidence: 99%

Long and branched polyamines are required for maintenance of the ribosome, tRNA^His and tRNA^Tyr in Thermus thermophilus cells at high temperatures

et al. 2017

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Thermus thermophilus is an extremely thermophilic eubacterium that produces various polyamines. Aminopropylagmatine ureohydrolase (SpeB) and SAM decarboxylase-like protein 1 (SpeD1) are involved in the biosynthesis of spermidine from arginine. Because long and branched polyamines in T. thermophilus are synthesized from spermidine, the speB and speD1 gene-deleted strains (DspeB and DspeD1, respectively) cannot synthesize long and branched polyamines. Although neither strain grew at high temperatures (>75°C) in minimal medium, both strains survived at 80°C when they were cultured at 70°C until the mid-log phase and then shifted to 80°C. We therefore prepared the DspeB and DspeD1 cells using this culture method. Microscopic analysis showed that both strains can survive for 10 h after the temperature shift. Although the modification levels of 2 0 -O-methylguanosine at position 18, N 7 -methylguanosine at position 46, 5-methyluridine at position 54 and N 1 -methyladenosine at position 58 in the class I tRNA from both strains were normal, amounts of tRNA Tyr , tRNA His , rRNAs and 70S ribosomes were decreased after the temperature shift. Furthermore, in vivo protein synthesis in both strains was completely lost 10 h after the temperature shift. Thus, long and branched polyamines are required for at least the maintenance of 70S ribosome and some tRNA species at high temperatures.

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“…At the same time, the enhanced agmatine production caused by organic acids may be associated with the mechanism of resistance to acidic environments, resembling the bacterial acid resistance system involving amino acid decarboxylation (39). During E. coli exposure to an acidic environment, a series of PLP-dependent decarboxylases (e.g., GadA/B and AdiA) decarboxylate glutamic acid and arginine to form GABA and agmatine, respectively, with a concomitant consumption of an intracellular proton (39)(40)(41). This contributes to the homeostatic maintenance of the cytoplasmic pH (39)(40)(41).…”

Section: Discussionmentioning

confidence: 99%

Agmatine Production by Aspergillus oryzae Is Elevated by Low pH during Solid-State Cultivation

Akasaka¹,

Kato

et al. 2018

Appl Environ Microbiol

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Sake (rice wine) produced by multiple parallel fermentation (MPF) involving (strain RW) and under solid-state cultivation conditions contained 3.5 mM agmatine, while that produced from enzymatically saccharified rice syrup by contained<0.01 mM agmatine. Agmatine was also produced in ethanol-free rice syrup prepared with under solid-state cultivation (3.1 mM) but not under submerged cultivation, demonstrating that in solid-state culture produces agmatine. The effect of cultivation conditions on agmatine production was examined. Agmatine production was boosted at 30°C and reached the highest level (6.3 mM) at pH 5.3. The addition of l-lactic, succinic, and citric acids reduced the initial culture pHs to 3.0, 3.5, and 3.2, respectively, resulting in a further increase in agmatine accumulation (8.2, 8.7, and 8.3 mM, respectively). Homogenate from a solid-state culture exhibited a maximum l-arginine decarboxylase (ADC) activity (74 pmol · min · μg) at pH 3.0 at 30°C; homogenate from a submerged culture exhibited an extremely low activity (<0.3 pmol · min · μg) under all conditions tested. These observations indicated that efficient agmatine production in ethanol-free rice syrup is achieved by an unidentified low-pH-dependent ADC induced during solid-state cultivation of , even though lacks ADC orthologs and instead possesses four ornithine decarboxylases (ODC1 to ODC4). Recombinant ODC1 and ODC2 exhibited no ADC activity at acidic pH (pH < 4.0), suggesting that other decarboxylases or an unidentified ADC is involved in agmatine production. It has been speculated that, in general, fungi do not synthesize agmatine from l-arginine because they do not possess genes encoding arginine decarboxylase. Numerous preclinical studies have shown that agmatine exerts pleiotropic effects on various molecular targets, leading to an improved quality of life. In the present study, we first demonstrated that l-arginine was a feasible substrate for agmatine production by the fungus RW. We observed that the productivity of agmatine by RW was elevated at low pH only during solid-state cultivation. is utilized in the production of various Asian fermented foods. The saccharification conditions optimized in the current study could be employed not only in the production of an agmatine-containing ethanol-free rice syrup but also in the production of many types of fermented foods, such as soy sauce (shoyu), rice vinegar, etc., as well as for use as novel therapeutic agents and nutraceuticals.

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Polyamines Stimulate the Level of the σ38 Subunit (RpoS) of Escherichia coli RNA Polymerase, Resulting in the Induction of the Glutamate Decarboxylase-dependent Acid Response System via the gadE Regulon

Cited by 25 publications

References 59 publications

The General Stress Response Is Conserved in Long-Term Soil-Persistent Strains of Escherichia coli

The General Stress Response Is Conserved in Long-Term Soil-Persistent Strains of Escherichia coli

Long and branched polyamines are required for maintenance of the ribosome, tRNA^His and tRNA^Tyr in Thermus thermophilus cells at high temperatures

Agmatine Production by Aspergillus oryzae Is Elevated by Low pH during Solid-State Cultivation

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Polyamines Stimulate the Level of the σ38 Subunit (RpoS) of Escherichia coli RNA Polymerase, Resulting in the Induction of the Glutamate Decarboxylase-dependent Acid Response System via the gadE Regulon

Cited by 25 publications

References 59 publications

The General Stress Response Is Conserved in Long-Term Soil-Persistent Strains of Escherichia coli

The General Stress Response Is Conserved in Long-Term Soil-Persistent Strains of Escherichia coli

Long and branched polyamines are required for maintenance of the ribosome, tRNAHis and tRNATyr in Thermus thermophilus cells at high temperatures

Agmatine Production by Aspergillus oryzae Is Elevated by Low pH during Solid-State Cultivation

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Long and branched polyamines are required for maintenance of the ribosome, tRNA^His and tRNA^Tyr in Thermus thermophilus cells at high temperatures