Open Access

Phenotypic and genomic survey on organic acid utilization profile of Pseudomonas mendocina strain S5.2, a vineyard soil isolate

  • Teik Min Chong1,
  • Jian-Woon Chen1, 2,
  • Wah-Seng See-Too1,
  • Choo-Yee Yu3,
  • Geik-Yong Ang3,
  • Yan Lue Lim1,
  • Wai-Fong Yin1,
  • Catherine Grandclément4,
  • Denis Faure4,
  • Yves Dessaux4 and
  • Kok-Gan Chan1, 2Email author
AMB Express20177:138

https://doi.org/10.1186/s13568-017-0437-7

Received: 24 March 2017

Accepted: 19 June 2017

Published: 26 June 2017

Abstract

Root exudates are chemical compounds that are released from living plant roots and provide significant energy, carbon, nitrogen and phosphorus sources for microbes inhabiting the rhizosphere. The exudates shape the microflora associated with the plant, as well as influences the plant health and productivity. Therefore, a better understanding of the trophic link that is established between the plant and the associated bacteria is necessary. In this study, a comprehensive survey on the utilization of grapevine and rootstock related organic acids were conducted on a vineyard soil isolate which is Pseudomonas mendocina strain S5.2. Phenotype microarray analysis has demonstrated that this strain can utilize several organic acids including lactic acid, succinic acid, malic acid, citric acid and fumaric acid as sole growth substrates. Complete genome analysis using single molecule real-time technology revealed that the genome consists of a 5,120,146 bp circular chromosome and a 252,328 bp megaplasmid. A series of genetic determinants associated with the carbon utilization signature of the strain were subsequently identified in the chromosome. Of note, the coexistence of genes encoding several iron–sulfur cluster independent isoenzymes in the genome indicated the importance of these enzymes in the events of iron deficiency. Synteny and comparative analysis have also unraveled the unique features of d-lactate dehydrogenase of strain S5.2 in the study. Collective information of this work has provided insights on the metabolic role of this strain in vineyard soil rhizosphere.

Keywords

Pseudomonas mendocina Single molecule real-time (SMRT) sequencing Vineyard soil Grapevine exudates Organic acids Carbon utilization enzymes

Introduction

Root exudates are rhizodeposits that are released from living plant roots into the surrounding rhizosphere (Uren 2007). These compounds mainly consisted of water-soluble sugars, organic acids, and amino acids, providing significant energy sources for microbes inhabiting the rhizosphere and its vicinity (Brimecombe et al. 2001). This represents a form of plant–microbe interaction that enables colonization and development of active microbial populations in plant roots and the surrounding soil (Bais et al. 2006; Haichar et al. 2008; Nihorimbere et al. 2011). Although the nature of exudates varies according to growth stages of a given plant, the composition of root exudates is also influenced by environmental factors such as pH, temperature, availability of nutrients, and presence of microorganisms (Nihorimbere et al. 2011; Singh and Mukerji 2006). Furthermore, the differences in exudation profiles directly impact the composition of the microflora inhabiting the specific niche that the rhizosphere is (Singh and Mukerji 2006; Mondy et al. 2014). The exudates shape the microflora associated with the plant, and further influences plant health and productivity, hence a better understanding of the trophic link that is established between the plant and the associated bacteria is necessary.

Grapevine (Vitis vinifera L.) is a non-climacteric fruit crop that grows as deep-rooted perennial plant (Archana et al. 2011). Pseudomonas spp. namely Pseudomonas fluorescens, P. lini, P. mendocina, P. putida, and P. syringae were among the soil inhabitants commonly found at both the acidic and alkaline soils of these native grapevines (Chan et al. 2016; Chenier et al. 2008; Chong et al. 2012, 2016; Karagöz et al. 2012). Our previous investigation on microbiota inhabiting the vineyard soil in Riquewihr, France has led to the isolation of P. mendocina strain S5.2 that harbor resistance traits towards various heavy metals (Chong et al. 2012).

In this study, a further elucidation of utilization of grapevine related compounds was conducted to gain insight on the intricate interaction occurring between the strain and the grapevine. Our work aimed at inclusively determining the phenotypic and genomic profiles associated with grapevine exudate utilization. With reference to the collective reports of various organic acids detected from grapevine and rootstock related exudates, a gene-trait matching approach followed by a comparative analysis was employed to unravel the complete profile of genetic determinants associated with the displayed utilization of the carbon compounds by this strain.

Materials and methods

Isolation and identification of bacteria

Pseudomonas mendocina strain S5.2 was isolated from a vineyard soil in Riquewihr, in the Alsace region of France. Isolation of this strain was performed using KG minimal medium as previously described (Chong et al. 2016). Routine maintenance of the culture was performed on Luria–Bertani (LB) (Merck, NJ, USA) medium at 28 °C.

Identification of the strain was conducted via 16S rRNA gene sequencing followed by phylogenetic analysis and pairwise similarity analysis using EzBioCloud database (http://www.ezbiocloud.net/identify) (Kim et al. 2012). Phylogenetic analysis was performed using molecular evolutionary genetic analysis (MEGA) version 6.06 (Tamura et al. 2013) with the list of hits from EzBioCloud 16S rRNA database. Scanning electron microscopy (SEM) observation of strain S5.2 was performed with osmium tetroxide fixing and ethanol dehydration procedures followed by viewing using a SEM TM3030 (Hitachi, Japan) device in accordance to Lau et al. (2014) with minor modification.

Phenotype microarray analysis

The carbon utilization profile of strain S5.2 was assessed using the 96-well PM1 and PM2A plates (Biolog, USA). In brief, the overnight cultured bacterial colonies were inoculated into IF-0a GN/GP base inoculating fluid (Biolog, USA) to reach 85% transmittance (T) according to the manufacturer’s protocol. Aliquots (100 µl) of cell suspension and 1× Biolog redox dye mix A were inoculated into each well of the plates respectively, followed by incubation at 28 °C. The utilization and growth of 192 different carbon substrates from the plates were monitored for 48 h with readings taken at 15 min intervals.

The kinetic information was recorded and quantified using OmniLog OL_FM_12 kinetic software (Biolog, USA) followed by data analysis (Bochner et al. 2001). In the event of bacterial growth, photographic readings of colour intensity resulted in dye reduction were represented in OmniLog units (OU) (Khatri et al. 2013). The threshold for positive bacterial growth was established at 100 OU, calculated with the subtraction of maximum growth value with the first reading (0 h).

Genome sequencing, assembly and annotation

Genomic DNA of P. mendocina S5.2 was purified using MasterPure DNA Purification Kit (Epicentre, Illumina Inc., Madison, Wisconsin, USA) followed by purity measurement and quantification using NanoDrop 2000™ spectrophotometer (Thermo Scientific, MA, USA) and Qubit 2.0® fluorometer (Life Technologies, MA, USA), respectively. Sequencing library was prepared from purified genomic DNA according to the guidelines of Template Preparation Kit (Pacific Biosciences, Inc., CA) with library size targeted at 20 kb. Sequence collection was then carried out in 2 SMRT cells using P6/C4 chemistry on a PacBio RS II platform (See-Too et al. 2016).

De novo assembly of the long reads was performed using the Hierarchical Genome Assembly Process (HGAP) version 2.0 using the PacBio SMRT portal. Gepard dotplot program (Krumsiek et al. 2007) was employed to verify the circularity of the resulted contigs followed by circularization of overlapping ends using minimus2 pipeline in AMOS software package (Treangen et al. 2011). Genome annotation was subsequently performed using Rapid Prokaryotic Genome Annotation (PROKKA)(Seemann 2014).

Bioinformatics analyses

Candidate genes potentially involved in the metabolism of carbon sources were validated using the rapid annotation subsystems technology (RAST) server (Aziz et al. 2008) and NCBI prokaryotic genome annotation pipeline (PGAP). Subsequently, MEGA version 6.06 was also employed for multiple sequence alignment of the amino acids. Additionally, pairwise average nucleotide identity (ANI) analysis using strain S5.2 and other relative Pseudomonas spp. was conducted using JSpeciesWS (http://jspecies.ribohost.com/jspeciesws/) with above cutoff more than 95% (Richter et al. 2016). Lastly, the synteny and comparative analysis on the genes of interest were conducted based on SyntTax web server using default parameter followed by manual verification (Oberto 2013).

Results

Properties of P. mendocina strain S5.2

SEM showed that cells of strain S5.2 were 1.5–2.5 µm in length and 0.8–1.0 µm in width (Additional file 1: Figure S1). Pairwise similarity analysis on EzBioCloud database followed by phylogenetic analysis using complete nucleotide sequences of 16S rRNA showed that strain S5.2 was closely related to P. mendocina NBRC 14162T (Additional file 2: Figure S2). This observation was later verified with ANIb analysis (Additional file 3: Table S1).

Organic acid utilization profiling

Among the 192 putative carbon sources tested, P. mendocina S5.2 was able to utilize 58 compounds as sole carbon sources. With reference to the grapevine and root exudates related organic acids, positive utilization was detected for l-lactic acid, succinic acid, d-malic acid, l-malic acid, d, l-malic acid, citric acid and fumaric acid, with average OU values at 243 ± 55 and growth value up to 293 with citric acid as sole carbon (Table 1). The inability of the strain to utilize oxalic, sorbic and all enantiomers of tartaric acids with average growth values of 26 ± 7 was also observed (Table 1).
Table 1

Utilization of grapevine and root exudates related compounds as sole carbon source by P. mendocina strain S5.2

Microplate

Plate position

Carbon source

Growth observed

Omnilog unit (OU)

PM1

A5

Succinic acid

+

288

 

B9

l-Lactic acid

+

257

 

C3

d, l-Malic acid

+

255

 

C7

d-Fructose

36

 

C9

α-d-Glucose

+

233

 

D11

Sucrose

32

 

E2

m-Tartaric acid

17

 

F2

Citric acid

+

293

 

F5

Fumaric acid

+

256

 

G11

d-Malic acid

+

126

 

G12

l-Malic acid

+

270

PM2A

C2

l-Glucose

22

 

D12

Butyric acid

+

159

 

F2

Malonic acid

+

206

 

F4

Oxalic acid

25

 

F9

Sorbic acid

21

 

F11

d-Tartaric acid

18

 

F12

l-Tartaric acid

21

Genome properties

The genome of P. mendocina S5.2 contained a ~ 5.12 Mb circular chromosome and a ~ 0.25 Mb megaplasmid that was later designated as pPME5. They were assembled in a single contig each with average coverages of 181.55× and 206.96× obtained for the chromosome and pPME5 plasmid, respectively. The mean G+C content of the chromosome (62.4%) was found to be higher than that of pPME5 (54.7%). Among the 4641 predicted protein coding genes, a total of 3747 (80.7%) could be associated with clear functions. In contrast, only 24 out of 319 (7.5%) open reading frames of pPME5 were predicted to have known functions (Table 2).
Table 2

General features of the P. mendocina strain S5.2 genome predicted in PGAP

Genetic elements

Chromosome

Plasmid pPME5

Size (bp)

5,120,146

252,328

G+C content (%)

62.4

54.7

Protein coding genes

4641

319

Genes with predicted functions

3747

24

rRNA genes (5S, 16S, 23S)

4, 4, 4

0, 0, 0

tRNA genes

66

4

Other RNA genes

4

0

Genomic features associated with organic acid utilization

The collective genomic and phenotypic information in the study has enabled the identification of genes for the specific carbon utilization. The circular chromosome of P. mendocina strain S5.2 was found to harbor a series of orthologous genes and operons associated with utilization traits of grapevine and root related organic acids (Fig. 1; Table 1).
Fig. 1

Organization and synteny of putative gene clusters and operons correlated to succinic, malic, fumaric and citric acids utilization of P. mendocina S5.2

For utilization of succinic acid, the sdhCDAB operon encoding succinate dehydrogenase (SDH) complex, a tricarboxylic (TCA) cycle enzyme was identified (Table 3). The reported catalysis of SDH involves the oxidation of succinate to fumarate, coupled with the reduction of ubiquinone to ubiquinol (Ackrell et al. 1992; Westenberg and Guerinot 1999).
Table 3

Identified ORFs in the chromosome associated with organic acid and sugar metabolism of P. mendocina strain S5.2

Locus tag

Annotation/predicted Role

ORF

Position in genome

Size (bp)

Orientation

Succinic acid (Succinate + ubiquinone → fumarate + ubiquinol)

DW68_012890

Succinate dehydrogenase (iron–sulfur subunit)

sdhB

2,790,535–2,791,242

708

DW68_012895

Succinate dehydrogenase (flavoprotein subunit)

sdhA

2,791,254–2,793,026

1773

DW68_012900

Succinate dehydrogenase (cytochrome b small subunit)

sdhD

2,793,030–2,793,398

369

DW68_012905

Succinate dehydrogenase (cytochrome b560 subunit)

sdhC

2,793,392–2,793,766

374

Lactic acid

DW68_005140

d-Lactate dehydrogenase

dld

1,090,088–1,091,806

1719

DW68_005145

l-Lactate dehydrogenase

lldD

1,091,811–1,092,950

1140

DW68_005150

l-Lactate permease

lldP

1,093,035–1,094,726

1692

DW68_005155

Lactate responsive regulator

lldR

1,095,022–1,095,789

768

Malic acid (malate  oxaloacetate)

DW68_020815

Malate dehydrogenase

sfcA

4,486,244–4,487,512

1269

Malic acid (malate → oxaloacetate)

DW68_008120

Malate:quinone oxidoreductase

mqo

1,719,586–1,721,193

1608

Fumaric acid (fumarate  Malate)

DW68_007085

Fumarate hydratase class I

fumA

1,503,228–1,504,751

1524

DW68_014875

Fumarate hydratase class II

fumC

3,205,005–3,206,399

1395

Citric acid (citrate → isocitrate)

DW68_010115

Aconitate hydratase A

acnA

2,182,629–2,185,370

2742

DW68_013280

Aconitate hydratase B

acnB

2,870,427–2,873,027

2601

Besides, an operon associated with lactic acid utilization encoding putative NAD-independent lactate dehydrogenase (iLDH) activity was also present. This enzyme possibly catalyzes the oxidation of lactate to pyruvate, a feature essential for most lactate-utilizing bacteria (Diez-Gonzalez et al. 1995; Gao et al. 2015; Gibello et al. 1999; Goffin et al. 2004). Components of this operon also included a lactate permease (lldP), l-lactate dehydrogenase (lldD) and d-lactate dehydrogenase gene (dld) indicating that strain S5.2 could degrade both lactate enantiomers (Table 3). Adjacent to these genes was lldR that encoded a transcriptional regulator possibly controlling the expression of the above-described genes. Comparative analysis with other Pseudomonas strains showed a high degree of synteny for the lldRPD genes (Fig. 2). Although sharing the identical flavin adenine dinucleotide (FAD)-binding site with all compared strains, sequence similarity search showed that the dld of strain 5.2 was similar only to those of some Pseudomonas spp., Alcaligenes spp., and Deftia spp. strains.
Fig. 2

Left phylogenetic analysis of putative d-lactate dehydrogenase (DLD) of strain S5.2 relative to other Pseudomonas, Alcaligenes faecalis and Deftia spp. Right comparison and synteny of lldRPD and dld genes among different strains. Positions of the compared DLD related genes in the phylogenetic tree were marked in respective shapes

The growth of P. mendocina strain S5.2 was observed in the presence of malic acid enantiomers. Two distinctive genes encoding malate dehydrogenase (SfcA) and malate quinone oxidoreductase (MQO) were found (Table 3). These enzymes shared a general activity catalyzing the oxidation of malate to oxaloacetate. SfcA is a cytoplasmic malate dehydrogenase that reversibly oxidizes malate and is a principal enzyme in the TCA cycle that requires nicotinamide adenine dinucleotide (NAD) as an electron acceptor (van der Rest et al. 2000). Alternatively, MQO is FAD-dependent, membrane associated protein that irreversibly oxidizes malate and donates electrons to quinones of the electron transfer chain (Kather et al. 2000).

Following the fumaric acid utilization phenotype, the genome also harbored genes encoding two classes of fumarate hydratase, namely FumA and FumC (Table 3). FumA is a class I fumarase that catalyzes the interconversion of fumarate to malate and requires iron–sulfur (Fe–S) cluster as a cofactor (Chenier et al. 2008; Flint et al. 1992). In contrast, FumC does not rely on Fe–S clusters for hydration of fumarate to malate (Chenier et al. 2008; Hassett et al. 1997). Coexistence of the isoenzymes in the genome may permit the strain to better survive under iron deficiency conditions. Genes for aconitate hydratases, AcnA and AcnB were also detected (Table 3) in the genome ensuing the proficient metabolism of citric acid reported above. Acn proteins catalyze the stereospecific isomerization of citrate to isocitrate and require Fe–S as an enzyme cofactor, as does FumA (Beinert and Kennedy 1993; Mailloux et al. 2006).

Discussion

The present work has demonstrated the carbon utilization signature of P. mendocina strain S5.2 in relation with in silico identification of genomic features associated with grapevine organic acid utilization. Tartaric, malic, oxalic, lactic, citric and succinic acids are among the main organic acids detected in grapevines and root exudates across various genotypes (Andersen and Brodbeck 1989; Cançado et al. 2009; Dharmadhikari 1994; Kliewer 1966; Li et al. 2013; López-Rayo et al. 2015; Mato et al. 2007). The illustrated utilization profile of these organic acids by P. mendocina strain S5.2 has provided new insights into the diversity of carbon utilization by P. mendocina. Subsequently, the gene-trait matching approach has demonstrated that these organic acids are catabolic substrates for the strain, involving the concerted actions of enzymes featured in TCA cycle and possibly other metabolic pathways. Such profile may also reflect on the specific nutrient requirements of the strain towards the given niche of the rhizosphere, in which the composition of the deposited exudates was affected by the aforementioned environmental factors (Nihorimbere et al. 2011; Singh and Mukerji 2006).

As an update on the previously reported draft genome of P. mendocina strain S5.2, the availability of complete genome sequences has allowed accurate definition of gene coordinates and recognition of paralogous gene families. Of note, the unique feature of DLD gene of strain S5.2 was highlighted in this study through amino acid sequence alignment and phylogenetic analysis. Despite sharing a high degree of synteny and similarity for genes encoding LldR, LldP and LldD, the DLD of strain S5.2 did not group with the putative DLD2/ferrodoxin of most Pseudomonas spp. Instead, the DLD of strain S5.2 shared higher similarity withs DLD of P. alcaliphila and other betaproteobacteria strains (Alcaligenes faecelis and Deftia sp.) (Fig. 2). Essentially, phylogenomic analysis conducted by Gomila and coworkers (2015) showed that P. mendocina and P. alcaliphila were in fact clustered under P. oleovorans group which is closely related to P. aeruginosa group. Hence such differential grouping of DLD even among the closely related groups of Pseudomonas might represent distintive catalytic mechanism required for d-lactate metabolism.

On the other hand, the identification of several isoenzymes has indicated differential catabolic preferences in relation with changes in environmental factors. For instance, the identification of Fe–S independent isoenzymes for utilization of malic acid, MQO and fumaric acid, FumC could be an indication of the essentiality of these enzymes during iron deficiency events. In addition, the absence of MQO has been shown to impede utilization of acetate, ethanol and acyclic terpenes in Pseudomonas strains, hence implying the essentiality of MQO in the metabolic versatility of strain S5.2 (Förster-Fromme and Jendrossek 2005; Kretzschmar et al. 2002).

Interestingly, strain S5.2 was shown to exhibit some resistance to copper (Chong et al. 2012). It is also possible to relate the carbon utilization profile with heavy metal resistance traits. Indeed, various carbon sources can serve as an effective electron donor for a given metal resistance, as observed with the reduction rate of hexavalent chromium [Cr(VI)] and trivalent iron [Fe(III)] by Cellulomonas sp. ES6 in presence of molasses versus pure sucrose (Field et al. 2013). Also, a combination of various carbon sources was required for chromium reduction by Klebsiella sp. PB6 and by a bacterial consortium in contaminated sediments (Smith et al. 2002; Wani and Omozele 2015). Given the heavy metal resistant traits displayed by Pseudomonas strains in previous studies (Chan et al. 2016; Chong et al. 2012, 2016), the preferences in utilizing the specific carbon compounds for in situ remediation of copper and other metal ions for instance in vineyard environments should be conducted in future research.

In conclusion, the present work has demonstrated the carbon utilization signature of P. mendocina strain S5.2, together with in silico identification of genomic features associated with grapevine organic acid utilization. Taken together with the relative cooper resistance identified earlier (Chong et al. 2012), this work demonstrates the remarkable adaptation of P. mendocina strain S5.2 to the grapevine and vineyards environment.

Abbreviations

ANI: 

average nucleotide identity

DLD: 

d-lactate dehydrogenase

FAD: 

flavin adenine dinucleotide

Fe–S: 

iron–sulfur

HGAP: 

Hierarchical Genome Assembly Process

iLDH: 

NAD-independent lactate dehydrogenases

LB: 

Luria–Bertani

LDH: 

lactate dehydrogenase

lldD: 

l-lactate dehydrogenase

lldP: 

lactate permease

MEGA: 

molecular evolutionary genetic analysis

MQO: 

malate quinone oxidoreductase

NAD: 

nicotinamide adenine dinucleotide

OU: 

OmniLog units

PGAP: 

prokaryotic genome annotation pipeline

PROKKA: 

rapid prokaryotic genome annotation

RAST: 

rapid annotation subsystems technology

SDH: 

succinate dehydrogenase

SEM: 

scanning electron microscopy

SfcA: 

malate dehydrogenase

SMRT: 

single molecule real-time

TCA: 

tricarboxylic

Declarations

Authors’ contributions

Design of the experiments: TMC, JWC, WSST, CG, YD, DF, KGC. Experiments performed by: TMC, JWC, CYY, GYA, YLL. Data analyses: TMC, JWC, WFY, CG, DF, YD, KGC. The article written by: TMC, JWC, WSST, YD, KGC. All authors read and approved the final manuscript.

Authors’ information

TMC, WSST, YLL, WFY are postgraduate students and officers from University of Malaya whereas CYY and GYA are from Universiti Teknologi MARA and their research work focus on genomic studies and bioinformatics. JWC is a postdoctoral fellow from University of Malaya specializes in phenotype microarray analysis. CG is a research engineer whereas DF and YD are research advisors from Centre National de la Recherche Scientifique (CNRS), France. Their area of expertise includes genomics, plant pathology and microbial ecology. At last, KGC is an Assoc. Prof. in University of Malaya and the director of UM Omics Centre. His area of expertise includes molecular microbiology, bacteriology and genomics studies.

Acknowledgements

KGC, TMC, and YD thank The French Embassy in Malaysia for the awarded fellowships and continuous support of the collaborative effort between the CNRS (Gif) and University of Malaya (KL) laboratories.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

All the data applied in the study are included in the tables and figures presented. The complete genome sequence has been deposited at NCBI under accession number CP013124 for the chromosome and CP013125 for the pPME5 plasmid. Strain deposition was conducted in German Collection of Microorganisms and Cell Cultures (DSMZ) with the deposition number of DSM102033.

Consent for publication

Informed consent was obtained from all individual participants of this study.

Funding

This research was supported by the University of Malaya through HIR Grants awarded to KGC (UM-MOHE HIR Grant UM C/625/1/HIR/MOHE/CHAN/14/1, No. H-50001-A000027; UM-MOHE HIR Grant UM C/625/1/HIR/MOHE/CHAN/01, No. A000001-50001). This research was also funded by Postgraduate Research Fund (PPP) (Grant No. PG080-2015B) awarded to TMC.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors’ Affiliations

(1)
Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya
(2)
UM Omics Centre, University of Malaya
(3)
Integrative Pharmacogenomics Institute (iPROMISE), Universiti Teknologi MARA
(4)
Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay

References

  1. Ackrell BAC, Johnson MK, Gunsalus RP, Cecchini G (1992) Structure and function of succinate dehydrogenase and fumarate reductase. In: Mueller F (ed) Chemistry and biochemistry of flavoenzymes, vol 3. CRC Press, Boca Raton, pp 229–297Google Scholar
  2. Andersen PC, Brodbeck BV (1989) Diurnal and temporal changes in the chemical profile of xylem exudate from Vitis rotundifolia. Physiol Plant 75:63–70View ArticleGoogle Scholar
  3. Archana S, Prabakar K, Raguchander T, Hubballi M, Valarmathi P, Prakasam V (2011) Defense responses of grapevine to Plasmopara viticola induced by azoxystrobin and Pseudomonas fluorescens. Int J Agric Sustain 3:30–38Google Scholar
  4. Aziz RK, Bartels D, Best AA, Dejongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75View ArticleGoogle Scholar
  5. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266View ArticlePubMedGoogle Scholar
  6. Beinert H, Kennedy MC (1993) Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB J 7:1442–1449PubMedGoogle Scholar
  7. Bochner BR, Gadzinski P, Panomitros E (2001) Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res 11:1246–1255View ArticlePubMedPubMed CentralGoogle Scholar
  8. Brimecombe MJ, de Leij FA, Lynch JM (2001) The effect of root exudates on rhizosphere microbial populations. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface. Marcel-Dekker, New York, pp 95–140Google Scholar
  9. Cançado GMA, Ribeiro AP, Piñeros MA, Miyata LY, Alvarenga ÂA, Villa F, Pasqual M, Purgatto E (2009) Evaluation of aluminium tolerance in grapevine rootstocks. Vitis 48:167–173Google Scholar
  10. Chan K-G, Chong T-M, Adrian T-G-S, Kher HL, Grandclément C, Faure D, Yin W-F, Dessaux Y, Hong K-W (2016) Pseudomonas lini strain ZBG1 revealed carboxylic acid utilization and copper resistance features required for adaptation to vineyard soil environment: a draft genome analysis. J Genom 4:26–28View ArticleGoogle Scholar
  11. Chenier D, Beriault R, Mailloux R, Baquie M, Abramia G, Lemire J, Appanna V (2008) Involvement of fumarase C and NADH oxidase in metabolic adaptation of Pseudomonas fluorescens cells evoked by aluminum and gallium toxicity. Appl Environ Microbiol 74:3977–3984View ArticlePubMedPubMed CentralGoogle Scholar
  12. Chong TM, Yin W-F, Mondy S, Grandclément C, Dessaux Y, Chan K-G (2012) Heavy-metal resistance of a France vineyard soil bacterium, Pseudomonas mendocina strain S5.2, revealed by whole-genome sequencing. J Bacteriol 194:6366View ArticlePubMedPubMed CentralGoogle Scholar
  13. Chong TM, Yin W-F, Chen J-W, Mondy S, Grandclément C, Faure D, Dessaux Y, Chan K-G (2016) Comprehensive genomic and phenotypic metal resistance profile of Pseudomonas putida strain S13.1.2 isolated from a vineyard soil. AMB Express 6:95View ArticlePubMedPubMed CentralGoogle Scholar
  14. Dharmadhikari M (1994) Composition of grapes. Vineyard Vintage View Mo State Univ 9:3–8Google Scholar
  15. Diez-Gonzalez F, Russell JB, Hunter JB (1995) The role of an NAD-independent lactate dehydrogenase and acetate in the utilization of lactate by Clostridium acetobutylicum strain P262. Arch Microbiol 164:36–42View ArticleGoogle Scholar
  16. FeZ Haichar, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230View ArticleGoogle Scholar
  17. Field EK, Gerlach R, Viamajala S, Jennings LK, Peyton BM, Apel WA (2013) Hexavalent chromium reduction by Cellulomonas sp. strain ES6: the influence of carbon source, iron minerals, and electron shuttling compounds. Biodegradation 24:437–450View ArticlePubMedGoogle Scholar
  18. Flint DH, Emptage MH, Guest JR (1992) Fumarase a from Escherichia coli: purification and characterization as an iron–sulfur cluster containing enzyme. Biochemistry 31:10331–10337View ArticlePubMedGoogle Scholar
  19. Förster-Fromme K, Jendrossek D (2005) Malate: quinone oxidoreductase (MqoB) is required for growth on acetate and linear terpenes in Pseudomonas citronellolis. FEMS Microbiol Lett 246:25–31View ArticlePubMedGoogle Scholar
  20. Gao C, Wang Y, Zhang Y, Lv M, Dou P, Xu P, Ma C (2015) NAD-independent l-lactate dehydrogenase required for l-lactate utilization in Pseudomonas stutzeri A1501. J Bacteriol 197:2239–2247View ArticlePubMedPubMed CentralGoogle Scholar
  21. Gibello A, Collins MD, Domínguez L, Fernández-Garayzábal JF, Richardson PT (1999) Cloning and analysis of the l-lactate utilization genes from Streptococcus iniae. Appl Environ Microbiol 65:4346–4350PubMedPubMed CentralGoogle Scholar
  22. Goffin P, Lorquet F, Kleerebezem M, Hols P (2004) Major role of NAD-dependent lactate dehydrogenases in aerobic lactate utilization in Lactobacillus plantarum during early stationary phase. J Bacteriol 186:6661–6666View ArticlePubMedPubMed CentralGoogle Scholar
  23. Gomila M, Peña A, Mulet M, Lalucat J, García-Valdés E (2015) Phylogenomics and systematics in Pseudomonas. Front Microbiol 6:214View ArticlePubMedPubMed CentralGoogle Scholar
  24. Hassett DJ, Howell ML, Sokol PA, Vasil ML, Dean GE (1997) Fumarase C activity is elevated in response to iron deprivation and in mucoid, alginate-producing Pseudomonas aeruginosa: cloning and characterization of fumC and purification of native fumC. J Bacteriol 179:1442–1451View ArticlePubMedPubMed CentralGoogle Scholar
  25. Karagöz K, Ateş F, Karagöz H, Kotan R, Çakmakçı R (2012) Characterization of plant growth-promoting traits of bacteria isolated from the rhizosphere of grapevine grown in alkaline and acidic soils. Eur J Soil Biol 50:144–150View ArticleGoogle Scholar
  26. Kather B, Stingl K, van der Rest ME, Altendorf K, Molenaar D (2000) Another unusual type of citric acid cycle enzyme in Helicobacter pylori: the malate: quinone oxidoreductase. J Bacteriol 182:3204–3209View ArticlePubMedPubMed CentralGoogle Scholar
  27. Khatri B, Fielder M, Jones G, Newell W, Abu-Oun M, Wheeler PR (2013) High throughput phenotypic analysis of Mycobacterium tuberculosis and Mycobacterium bovis strains’ metabolism using biolog phenotype microarrays. PLoS ONE 8:e52673View ArticlePubMedPubMed CentralGoogle Scholar
  28. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721View ArticlePubMedGoogle Scholar
  29. Kliewer WM (1966) Sugars and organic acids of Vitis vinifera. Plant Physiol 41:923–931View ArticlePubMedPubMed CentralGoogle Scholar
  30. Kretzschmar U, Rückert A, Jeoung J-H, Görisch H (2002) Malate: quinone oxidoreductase is essential for growth on ethanol or acetate in Pseudomonas aeruginosa. Microbiology 148:3839–3847View ArticlePubMedGoogle Scholar
  31. Krumsiek J, Arnold R, Rattei T (2007) Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23:1026–1028View ArticlePubMedGoogle Scholar
  32. Lau YY, Yin W-F, Chan K-G (2014) Enterobacter asburiae strain L1: complete genome and whole genome optical mapping analysis of a quorum sensing bacterium. Sensors 14:13913–13924View ArticlePubMedPubMed CentralGoogle Scholar
  33. Li K, Guo XW, Xie HG, Guo Y, Li C (2013) Influence of root exudates and residues on soil microecological environment. Pak J Bot 45:1773–1779Google Scholar
  34. López-Rayo S, Foggia MD, Moreira ER, Donnini S, Bombai G, Filippini G, Pisis A, Rombolà AD (2015) Physiological responses in roots of the grapevine rootstock 140 Ruggeri subjected to Fe deficiency and Fe-heme nutrition. Plant Physiol Biochem 96:171–179View ArticlePubMedGoogle Scholar
  35. Mailloux RJ, Hamel R, Appanna VD (2006) Aluminum toxicity elicits a dysfunctional TCA cycle and succinate accumulation in hepatocytes. J Biochem Mol Toxicol 20:198–208View ArticlePubMedGoogle Scholar
  36. Mato I, Suárez-Luque S, Huidobro JF (2007) Simple determination of main organic acids in grape juice and wine by using capillary zone electrophoresis with direct UV detection. Food Chem 102:104–112View ArticleGoogle Scholar
  37. Mondy S, Lenglet A, Beury-Cirou A, Libanga C, Ratet P, Faure D, Dessaux Y (2014) An increasing opine carbon bias in artificial exudation systems and genetically modified plant rhizospheres leads to an increasing reshaping of bacterial populations. Mol Ecol 23:4846–4861View ArticlePubMedGoogle Scholar
  38. Nihorimbere V, Ongena M, Smargiassi M, Thonart P (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol Agron Soc Environ 15:327–337Google Scholar
  39. Oberto J (2013) SyntTax: a web server linking synteny to prokaryotic taxonomy. BMC Bioinformatics 14:4View ArticlePubMedPubMed CentralGoogle Scholar
  40. Richter M, Rosselló-Móra R, Glöckner FO, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 36:929–931View ArticleGoogle Scholar
  41. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069View ArticlePubMedGoogle Scholar
  42. See-Too W-S, Convey P, Pearce DA, Lim YL, Ee R, Yin W-F, Chan K-G (2016) Complete genome of Planococcus rifietoensis M8T, a halotolerant and potentially plant growth promoting bacterium. J Biotechnol 221:114–115View ArticlePubMedGoogle Scholar
  43. Singh G, Mukerji KG (2006) Root exudates as determinant of rhizospheric microbial biodiversity. In: Mukerji KG, Manoharachary C, Singh J (eds) Microbial activity in the rhizoshere. Springer, Berlin, pp 39–54View ArticleGoogle Scholar
  44. Smith WA, Apel WA, Petersen JN, Peyton BM (2002) Effect of carbon and energy source on bacterial chromate reduction. Bioremediat J 6:205–215View ArticleGoogle Scholar
  45. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729View ArticlePubMedPubMed CentralGoogle Scholar
  46. Treangen TJ, Sommer DD, Angly FE, Koren S, Pop M (2011) Next generation sequence assembly with AMOS. Curr Protoc Bioinform 33:11.8.1–11.8.18Google Scholar
  47. Uren NC (2007) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface, 2nd edn. CRC Press, Boca Raton, pp 1–21Google Scholar
  48. van der Rest ME, Frank C, Molenaar D (2000) Functions of the membrane-associated and cytoplasmic malate dehydrogenases in the citric acid cycle of Escherichia coli. J Bacteriol 182:6892–6899View ArticlePubMedPubMed CentralGoogle Scholar
  49. Wani PA, Omozele AB (2015) Cr(VI) removal by indigenous Klebsiella species PB6 isolated from contaminated soil under the influence of various factors. Curr Res Bacteriol 8:62–69View ArticleGoogle Scholar
  50. Westenberg DJ, Guerinot ML (1999) Succinate dehydrogenase (Sdh) from Bradyrhizobium japonicum is closely related to mitochondrial Sdh. J Bacteriol 181:4676–4679PubMedPubMed CentralGoogle Scholar

Copyright

© The Author(s) 2017