The Chaperone and Redox Properties of CnoX Chaperedoxins Are Tailored to the Proteostatic Needs of Bacterial Species

ABSTRACT Hypochlorous acid (bleach), an oxidizing compound produced by neutrophils, turns the Escherichia coli chaperedoxin CnoX into a powerful holdase protecting its substrates from bleach-induced aggregation. CnoX is well conserved in bacteria, even in non-infectious species unlikely to encounter this oxidant, muddying the role of CnoX in these organisms. Here, we found that CnoX in the non-pathogenic aquatic bacterium Caulobacter crescentus functions as a holdase that efficiently protects 50 proteins from heat-induced aggregation. Remarkably, the chaperone activity of Caulobacter CnoX is constitutive. Like E. coli CnoX, Caulobacter CnoX transfers its substrates to DnaK/J/GrpE and GroEL/ES for refolding, indicating conservation of cooperation with GroEL/ES. Interestingly, Caulobacter CnoX exhibits thioredoxin oxidoreductase activity, by which it controls the redox state of 90 proteins. This function, which E. coli CnoX lacks, is likely welcome in a bacterium poorly equipped with antioxidant defenses. Thus, the redox and chaperone properties of CnoX chaperedoxins were fine-tuned during evolution to adapt these proteins to the specific needs of each species. IMPORTANCE How proteins are protected from stress-induced aggregation is a crucial question in biology and a long-standing mystery. While a long series of landmark studies have provided important contributions to our current understanding of the proteostasis network, key fundamental questions remain unsolved. In this study, we show that the intrinsic features of the chaperedoxin CnoX, a folding factor that combines chaperone and redox protective function, have been tailored during evolution to fit to the specific needs of their host. Whereas Escherichia coli CnoX needs to be activated by bleach, a powerful oxidant produced by our immune system, its counterpart in Caulobacter crescentus, a bacterium living in bleach-free environments, is a constitutive chaperone. In addition, the redox properties of E. coli and C. crescentus CnoX also differ to best contribute to their respective cellular redox homeostasis. This work demonstrates how proteins from the same family have evolved to meet the needs of their hosts.

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Identification of Escherichia coli and Shigella Species from Whole-Genome Sequences

Journal of Clinical Microbiology ◽

10.1128/jcm.01790-16 ◽

2016 ◽

Vol 55 (2) ◽

pp. 616-623 ◽

Cited By ~ 49

Author(s):

Marie A. Chattaway ◽

Ulf Schaefer ◽

Rediat Tewolde ◽

Timothy J. Dallman ◽

Claire Jenkins

Keyword(s):

Escherichia Coli ◽

Clonal Complex ◽

Shigella Flexneri ◽

Bacterial Species ◽

Whole Genome ◽

Content Type ◽

E Coli ◽

Shigella Species ◽

Close Phylogenetic Relationship ◽

Initial Identification

ABSTRACTEscherichia coliandShigellaspecies are closely related and genetically constitute the same species. Differentiating between these two pathogens and accurately identifying the four species ofShigellaare therefore challenging. The organism-specific bioinformatics whole-genome sequencing (WGS) typing pipelines at Public Health England are dependent on the initial identification of the bacterial species by use of a kmer-based approach. Of the 1,982Escherichia coliandShigellasp. isolates analyzed in this study, 1,957 (98.4%) had concordant results by both traditional biochemistry and serology (TB&S) and the kmer identification (ID) derived from the WGS data. Of the 25 mismatches identified, 10 were enteroinvasiveE. coliisolates that were misidentified asShigella flexneriorS. boydiiby the kmer ID, and 8 wereS. flexneriisolates misidentified by TB&S asS. boydiidue to nonfunctionalS. flexneriO antigen biosynthesis genes. Analysis of the population structure based on multilocus sequence typing (MLST) data derived from the WGS data showed that the remaining discrepant results belonged to clonal complex 288 (CC288), comprising bothS. boydiiandS. dysenteriaestrains. Mismatches between the TB&S and kmer ID results were explained by the close phylogenetic relationship between the two species and were resolved with reference to the MLST data.Shigellacan be differentiated fromE. coliand accurately identified to the species level by use of kmer comparisons and MLST. Analysis of the WGS data provided explanations for the discordant results between TB&S and WGS data, revealed the true phylogenetic relationships between different species ofShigella, and identified emerging pathoadapted lineages.

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Tumble Suppression Is a Conserved Feature of Swarming Motility

mBio ◽

10.1128/mbio.01189-20 ◽

2020 ◽

Vol 11 (3) ◽

Author(s):

Jonathan D. Partridge ◽

Nguyen T. Q. Nhu ◽

Yann S. Dufour ◽

Rasika M. Harshey

Keyword(s):

Escherichia Coli ◽

Bacterial Species ◽

Behavioral Adaptation ◽

Diverse Group ◽

Swarming Motility ◽

Gram Negative ◽

Content Type ◽

E Coli ◽

Surfactant Secretion ◽

Motility Parameters

ABSTRACT Many bacteria use flagellum-driven motility to swarm or move collectively over a surface terrain. Bacterial adaptations for swarming can include cell elongation, hyperflagellation, recruitment of special stator proteins, and surfactant secretion, among others. We recently demonstrated another swarming adaptation in Escherichia coli, wherein the chemotaxis pathway is remodeled to decrease tumble bias (increase run durations), with running speeds increased as well. We show here that the modification of motility parameters during swarming is not unique to E. coli but is shared by a diverse group of bacteria we examined—Proteus mirabilis, Serratia marcescens, Salmonella enterica, Bacillus subtilis, and Pseudomonas aeruginosa—suggesting that increasing run durations and speeds are a cornerstone of swarming. IMPORTANCE Bacteria within a swarm move characteristically in packs, displaying an intricate swirling motion in which hundreds of dynamic rafts continuously form and dissociate as the swarm colonizes an increasing expanse of territory. The demonstrated property of E. coli to reduce its tumble bias and hence increase its run duration during swarming is expected to maintain and promote side-by-side alignment and cohesion within the bacterial packs. In this study, we observed a similar low tumble bias in five different bacterial species, both Gram positive and Gram negative, each inhabiting a unique habitat and posing unique problems to our health. The unanimous display of an altered run-tumble bias in swarms of all species examined in this investigation suggests that this behavioral adaptation is crucial for swarming.

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Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli: TABLE 1

Journal of Bacteriology ◽

10.1128/jb.00424-15 ◽

2015 ◽

Vol 198 (1) ◽

pp. 7-11 ◽

Cited By ~ 48

Author(s):

Regine Hengge ◽

Michael Y. Galperin ◽

Jean-Marc Ghigo ◽

Mark Gomelsky ◽

Jeffrey Green ◽

...

Keyword(s):

Escherichia Coli ◽

Molecular Mechanisms ◽

Bacterial Species ◽

Content Type ◽

E Coli ◽

Diguanylate Cyclases ◽

Genes Encoding ◽

Systematic Nomenclature ◽

K 12 ◽

Encoding Genes

In recent years,Escherichia colihas served as one of a few model bacterial species for studying cyclic di-GMP (c-di-GMP) signaling. The widely usedE. coliK-12 laboratory strains possess 29 genes encoding proteins with GGDEF and/or EAL domains, which include 12 diguanylate cyclases (DGC), 13 c-di-GMP-specific phosphodiesterases (PDE), and 4 “degenerate” enzymatically inactive proteins. In addition, six new GGDEF and EAL (GGDEF/EAL) domain-encoding genes, which encode two DGCs and four PDEs, have recently been found in genomic analyses of commensal and pathogenicE. colistrains. As a group of researchers who have been studying the molecular mechanisms and the genomic basis of c-di-GMP signaling inE. coli, we now propose a general and systematicdgcandpdenomenclature for the enzymatically active GGDEF/EAL domain-encoding genes of this model species. This nomenclature is intuitive and easy to memorize, and it can also be applied to additional genes and proteins that might be discovered in various strains ofE. coliin future studies.

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Lineage-Specific Distribution of Insertion Sequence Excision Enhancer in Enterotoxigenic Escherichia coli Isolated from Swine

Applied and Environmental Microbiology ◽

10.1128/aem.03696-13 ◽

2013 ◽

Vol 80 (4) ◽

pp. 1394-1402 ◽

Cited By ~ 7

Author(s):

Masahiro Kusumoto ◽

Dai Fukamizu ◽

Yoshitoshi Ogura ◽

Eiji Yoshida ◽

Fumiko Yamamoto ◽

...

Keyword(s):

Escherichia Coli ◽

Bacterial Species ◽

Bacterial Genome ◽

Enterotoxigenic Escherichia Coli ◽

Content Type ◽

E Coli ◽

Genomic Deletions ◽

Specific Distribution ◽

Multiple Copies ◽

Genomic Locations

ABSTRACTInsertion sequences (ISs) are the simplest transposable elements and are widely distributed in bacteria; however, they also play important roles in genome evolution. We recently identified a protein called IS excision enhancer (IEE) in enterohemorrhagicEscherichia coli(EHEC) O157. IEE promotes the excision of IS elements belonging to the IS3family, such as IS629, as well as several other families. IEE-mediated IS excision generates various genomic deletions that lead to the diversification of the bacterial genome. IEE has been found in a broad range of bacterial species; however, among sequencedE. colistrains, IEE is primarily found in EHEC isolates. In this study, we investigated non-EHEC pathogenicE. colistrains isolated from domestic animals and found that IEE is distributed in specific lineages of enterotoxigenicE. coli(ETEC) strains of serotypes O139 or O149 isolated from swine. Theieegene is located within integrative elements that are similar to SpLE1 of EHEC O157. Alliee-positive ETEC lineages also contained multiple copies of IS629, a preferred substrate of IEE, and their genomic locations varied significantly between strains, as observed in O157. These data suggest that IEE may have been transferred among EHEC and ETEC in swine via SpLE1 or SpLE1-like integrative elements. In addition, IS629is actively moving in the ETEC O139 and O149 genomes and, as in EHEC O157, is promoting the diversification of these genomes in combination with IEE.

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Unexpected Diversity of Escherichia coli SialateO-Acetyl Esterase NanS

Journal of Bacteriology ◽

10.1128/jb.00189-16 ◽

2016 ◽

Vol 198 (20) ◽

pp. 2803-2809 ◽

Cited By ~ 8

Author(s):

Ariel Rangel ◽

Susan M. Steenbergen ◽

Eric R. Vimr

Keyword(s):

Escherichia Coli ◽

Sialic Acid ◽

Bacterial Species ◽

Sialic Acids ◽

Host Bacterium ◽

Acetyl Esterase ◽

Content Type ◽

E Coli ◽

Host Microbe Interactions ◽

K 12

ABSTRACTThe sialic acids (N-acylneuraminates) are a group of nine-carbon keto-sugars existing mainly as terminal residues on animal glycoprotein and glycolipid carbohydrate chains. Bacterial commensals and pathogens exploit host sialic acids for nutrition, adhesion, or antirecognition, whereN-acetyl- orN-glycolylneuraminic acids are the two predominant chemical forms of sialic acids. Each form may be modified by acetyl esters at carbon position 4, 7, 8, or 9 and by a variety of less-common modifications. Modified sialic acids produce challenges for colonizing bacteria, because the chemical alterations toN-acetylneuraminic acid (Neu5Ac) confer increased resistance to sialidase and aldolase activities essential for the catabolism of host sialic acids. Bacteria withO-acetyl sialate esterase(s) utilize acetylated sialic acids for growth, thereby gaining a presumed metabolic advantage over competitors lacking this activity. Here, we demonstrate the esterase activity ofEscherichia coliNanS after purifying it as a C-terminal HaloTag fusion. Using a similar approach, we show thatE. colistrain O157:H7 Stx prophage or prophage remnants invariably include paralogs ofnanSoften located downstream of the Shiga-like toxin genes. These paralogs may include sequences encoding N- or C-terminal domains of unknown function where the NanS domains can act as sialateO-acetyl esterases, as shown by complementation of anE. colistrain K-12nanSmutant and the unimpaired growth of anE. coliO157nanSmutant onO-acetylated sialic acid. We further demonstrate thatnanShomologs inStreptococcusspp. also encode active esterase, demonstrating an unexpected diversity of bacterial sialateO-acetyl esterase.IMPORTANCEThe sialic acids are a family of over 40 naturally occurring 9-carbon keto-sugars that function in a variety of host-bacterium interactions. These sugars occur primarily as terminal carbohydrate residues on host glycoproteins and glycolipids. Available evidence indicates that diverse bacterial species use host sialic acids for adhesion or as sources of carbon and nitrogen. Our results show that the catabolism of the diacetylated form of host sialic acid requires a specialized esterase, NanS. Our results further show thatnanShomologs exist in bacteria other thanEscherichia coli, as well as part of toxigenicE. coliprophage. The unexpected diversity of these enzymes suggests new avenues for investigating host-bacterium interactions. Therefore, these original results extend our previous studies ofnanSto include mucosal pathogens, prophage, and prophage remnants. This expansion of thenanSsuperfamily suggests important, although as-yet-unknown, functions in host-microbe interactions.

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Impact of Metazooplankton Filter Feeding on Escherichia coli under Variable Environmental Conditions

Applied and Environmental Microbiology ◽

10.1128/aem.02006-19 ◽

2019 ◽

Vol 85 (23) ◽

Cited By ~ 1

Author(s):

Niveen S. Ismail ◽

Brittney M. Blokker ◽

Tyler R. Feeney ◽

Ruby H. Kohn ◽

Jingyi Liu ◽

...

Keyword(s):

Escherichia Coli ◽

Water Quality ◽

Surface Waters ◽

Environmental Variables ◽

Bacterial Species ◽

Clearance Rates ◽

Filter Feeding ◽

Fecal Indicator ◽

Content Type ◽

E Coli

ABSTRACT The fecal indicator bacterial species Escherichia coli is an important measure of water quality and a leading cause of impaired surface waters. We investigated the impact of the filter-feeding metazooplankton Daphnia magna on the inactivation of E. coli. The E. coli clearance rates of these daphnids were calculated from a series of batch experiments conducted under variable environmental conditions. Batch system experiments of 24 to 48 h in duration were completed to test the impacts of bacterial concentration, organism density, temperature, and water type. The maximum clearance rate for adult D. magna organisms was 2 ml h−1 organism−1. Less than 5% of E. coli removed from water by daphnids was recoverable from excretions. Sorption of E. coli on daphnid carapaces was not observed. As a comparison, the clearance rates of the freshwater rotifer Branchionus calyciflorus were also calculated for select conditions. The maximum clearance rate for B. calyciflorus was 6 × 10−4 ml h−1 organism−1. This research furthers our understanding of the impacts of metazooplankton predation on E. coli inactivation and the effects of environmental variables on filter feeding. Based on our results, metazooplankton can play an important role in the reduction of E. coli in natural treatment systems under environmentally relevant conditions. IMPORTANCE Escherichia coli is a fecal indicator bacterial species monitored by the U.S. Environmental Protection Agency to assess microbial water quality. Due to the potential human health implications linked to high levels of E. coli, it is important to understand the inactivation or reduction mechanisms in surface waters. Our research examines the capacities of two types of widespread filter-feeding freshwater metazooplankton, Daphnia magna and Brachionus calyciflorus, to reduce E. coli concentrations. We examine the impacts of different environmentally relevant conditions on the clearance rates. Our results contribute to a better understanding of the importance of metazooplankton in controlling E. coli concentrations and what conditions will reduce or increase grazing. These results provide baseline data to support future efforts to develop a quantitative model relating zooplankton uptake rates to relevant environmental variables.

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A New Player at the Flagellar Motor: FliL Controls both Motor Output and Bias

mBio ◽

10.1128/mbio.02367-14 ◽

2015 ◽

Vol 6 (2) ◽

Cited By ~ 28

Author(s):

Jonathan D. Partridge ◽

Vincent Nieto ◽

Rasika M. Harshey

Keyword(s):

Caulobacter Crescentus ◽

Bacterial Species ◽

Motor Output ◽

Structural Defects ◽

Stalk Cell ◽

Switching Frequency ◽

Content Type ◽

Bacterial Flagellum ◽

E Coli ◽

Flagellar Filament

ABSTRACT The bacterial flagellum is driven by a bidirectional rotary motor, which propels bacteria to swim through liquids or swarm over surfaces. While the functions of the major structural and regulatory components of the flagellum are known, the function of the well-conserved FliL protein is not. In Salmonella and Escherichia coli, the absence of FliL leads to a small defect in swimming but complete elimination of swarming. Here, we tracked single motors of these bacteria and found that absence of FliL decreases their speed as well as switching frequency. We demonstrate that FliL interacts strongly with itself, with the MS ring protein FliF, and with the stator proteins MotA and MotB and weakly with the rotor switch protein FliG. These and other experiments show that FliL increases motor output either by recruiting or stabilizing the stators or by increasing their efficiency and contributes additionally to torque generation at higher motor loads. The increased torque enabled by FliL explains why this protein is essential for swarming on an agar surface expected to offer increased resistance to bacterial movement. IMPORTANCE FliL is a well-conserved bacterial flagellar protein whose absence leads to a variety of motility defects, ranging from moderate to complete inhibition of swimming in some bacterial species, inhibition of swarming in others, structural defects that break the flagellar rod during swarming in E. coli and Salmonella, and failure to eject the flagellar filament during the developmental transition of a swimmer to a stalk cell in Caulobacter crescentus. Despite these many phenotypes, a specific function for FliL has remained elusive. Here, we established a central role for FliL at the Salmonella and E. coli motors, where it interacts with both rotor and stator proteins, increases motor output, and contributes to the normal rotational bias of the motor.

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Growth of Escherichia coli in Model Distribution System Biofilms Exposed to Hypochlorous Acid or Monochloramine

Applied and Environmental Microbiology ◽

10.1128/aem.69.9.5463-5471.2003 ◽

2003 ◽

Vol 69 (9) ◽

pp. 5463-5471 ◽

Cited By ~ 67

Author(s):

Margaret M. Williams ◽

Ellen B. Braun-Howland

Keyword(s):

Escherichia Coli ◽

Legionella Pneumophila ◽

Distribution System ◽

Distribution Systems ◽

Hypochlorous Acid ◽

Bacterial Species ◽

Phylogenetic Groups ◽

Bacterial Populations ◽

E Coli ◽

Model Distribution

ABSTRACT Bacteria indigenous to water distribution systems were used to grow multispecies biofilms within continuous-flow slide chambers. Six flow chambers were also inoculated with an Escherichia coli isolate obtained from potable water. The effect of disinfectants on bacterial populations was determined after exposure of established biofilms to 1 ppm of hypochlorous acid (ClOH) for 67 min or 4 ppm of monochloramine (NH2Cl) for 155 min. To test the ability of bacterial populations to initiate biofilm formation in the presence of disinfectants, we assessed the biofilms after 2 weeks of exposure to residual concentrations of 0.2 ppm of ClOH or 4 ppm of NH2Cl. Lastly, to determine the effect of recommended residual concentrations on newly established biofilms, we treated systems with 0.2 ppm of ClOH after 5 days of growth in the absence of disinfectant. Whole-cell in situ hybridizations using fluorescently tagged, 16S rRNA-targeted oligonucleotide probes performed on cryosectioned biofilms permitted the direct observation of metabolically active bacterial populations, including certain phylogenetic groups and species. The results of these studies confirmed the resistance of established bacterial biofilms to treatment with recommended levels of disinfectants. Specifically, Legionella pneumophila, E. coli, and β and δ proteobacteria were identified within biofilms both before and after treatment. Furthermore, although it was undetected using routine monitoring techniques, the observation of rRNA-containing E. coli within biofilms demonstrated not only survival but also metabolic activity of this organism within the model distribution systems. The persistence of diverse bacterial species within disinfectant-treated biofilms suggests that current testing practices underestimate the risk to immunocompromised individuals of contracting waterborne disease.

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Autoinducer 2-DependentEscherichia coliBiofilm Formation Is Enhanced in a Dual-Species Coculture

Applied and Environmental Microbiology ◽

10.1128/aem.02638-17 ◽

2017 ◽

Vol 84 (5) ◽

Cited By ~ 12

Author(s):

Leanid Laganenka ◽

Victor Sourjik

Keyword(s):

Escherichia Coli ◽

Stress Resistance ◽

Bacterial Species ◽

Interspecies Communication ◽

Content Type ◽

Collective Behaviors ◽

E Coli ◽

Autoinducer 2 ◽

Cell Densities

ABSTRACTBiofilms in nature typically consist of multiple species, and microbial interactions are likely to have crucial effects on biofilm development, structure, and functions. The best-understood form of communication within bacterial communities involves the production, release, and detection of signal molecules (autoinducers), known as quorum sensing. Although autoinducers mainly promote intraspecies communication, autoinducer 2 (AI-2) is produced and detected by a variety of bacteria, thus principally allowing interspecies communication. Here we show the importance of AI-2-mediated signaling in the formation of mixed biofilms byEnterococcus faecalisandEscherichia coli. Our results demonstrate that AI-2 produced byE. faecalispromotes collective behaviors ofE. coliat lower cell densities, enhancing autoaggregation ofE. colibut also leading to chemotaxis-dependent coaggregation between the two species. Finally, we show that formation of such mixed dual-species biofilms increases the stress resistance of bothE. coliandE. faecalis.IMPORTANCEThe role of interspecies communication in the development of mixed microbial communities is becoming increasingly apparent, but specific examples of such communication remain limited. The universal signal molecule AI-2 is well known to regulate cell-density-dependent phenotypes of many bacterial species but, despite its potential for interspecies communication, the role of AI-2 in the establishment of multispecies communities is not well understood. In this study, we explore AI-2 signaling in a dual-species community containing two bacterial species that naturally cooccur in their mammalian hosts, i.e.,Escherichia coliandEnterococcus faecalis. We show that active production of AI-2 byE. faecalisallowsE. colito perform collective behaviors at low cell densities. Additionally, AI-2- and chemotaxis-dependent coaggregation withE. faecaliscreates nucleation zones for rapid growth ofE. colimicrocolonies in mixed biofilms and enhances the stress resistance of both species.

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Genome-Based Comparison of Cyclic Di-GMP Signaling in Pathogenic and Commensal Escherichia coli Strains

Journal of Bacteriology ◽

10.1128/jb.00520-15 ◽

2015 ◽

Vol 198 (1) ◽

pp. 111-126 ◽

Cited By ~ 28

Author(s):

Tatyana L. Povolotsky ◽

Regine Hengge

Keyword(s):

Escherichia Coli ◽

Bacterial Species ◽

Content Type ◽

E Coli ◽

Large Deletions ◽

Diguanylate Cyclases ◽

Core Set ◽

Genes Encoding ◽

K 12 ◽

Encoding Genes

ABSTRACTThe ubiquitous bacterial second messenger cyclic di-GMP (c-di-GMP) has recently become prominent as a trigger for biofilm formation in many bacteria. It is generated by diguanylate cyclases (DGCs; with GGDEF domains) and degraded by specific phosphodiesterases (PDEs; containing either EAL or HD-GYP domains). Most bacterial species contain multiples of these proteins with some having specific functions that are based on direct molecular interactions in addition to their enzymatic activities.Escherichia coliK-12 laboratory strains feature 29 genes encoding GGDEF and/or EAL domains, resulting in a set of 12 DGCs, 13 PDEs, and four enzymatically inactive “degenerate” proteins that act by direct macromolecular interactions. We present here a comparative analysis of GGDEF/EAL domain-encoding genes in 61 genomes of pathogenic, commensal, and probioticE. colistrains (including enteric pathogens such as enteroaggregative, enterohemorrhagic, enteropathogenic, enterotoxigenic, and adherent and invasiveEscherichia coliand the 2011 German outbreak O104:H4 strain, as well as extraintestinal pathogenicE. coli, such as uropathogenic and meningitis-associatedE. coli). We describe additional genes for two membrane-associated DGCs (DgcX and DgcY) and four PDEs (the membrane-associated PdeT, as well as the EAL domain-only proteins PdeW, PdeX, and PdeY), thus showing the pangenome ofE. colito contain at least 35 GGDEF/EAL domain proteins. A core set of only eight proteins is absolutely conserved in all 61 strains: DgcC (YaiC), DgcI (YliF), PdeB (YlaB), PdeH (YhjH), PdeK (YhjK), PdeN (Rtn), and the degenerate proteins CsrD and CdgI (YeaI). In all other GGDEF/EAL domain genes, diverse point and frameshift mutations, as well as small or large deletions, were discovered in various strains.IMPORTANCEOur analysis reveals interesting trends in pathogenicEscherichia colithat could reflect different host cell adherence mechanisms. These may either benefit from or be counteracted by the c-di-GMP-stimulated production of amyloid curli fibers and cellulose. Thus, EAEC, which adhere in a “stacked brick” biofilm mode, have a potential for high c-di-GMP accumulation due to DgcX, a strongly expressed additional DGC. In contrast, EHEC and UPEC, which use alternative adherence mechanisms, tend to have extra PDEs, suggesting that low cellular c-di-GMP levels are crucial for these strains under specific conditions. Overall, our study also indicates that GGDEF/EAL domain proteins evolve rapidly and thereby contribute to adaptation to host-specific and environmental niches of various types ofE. coli.

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