A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti

Draghi WO, Del Papa MF, Hellweg C, Watt SA, Watt TF, Barsch A, Lozano MJ, Lagares, A. J, Salas ME, Lopez JL, Albicoro FJ, et al. (2016)

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Draghi, W. O.; Del Papa, M. F.; Hellweg, C.; Watt, S. A.; Watt, T. F.; Barsch, A.; Lozano, M. J.; Lagares, A., Jr.; Salas, M. E.; Lopez, J. L.; Albicoro, F. J.; Nilsson, J. F.
Abstract / Bemerkung
Abiotic stresses in general and extracellular acidity in particular disturb and limit nitrogen-fixing symbioses between rhizobia and their host legumes. Except for valuable molecular-biological studies on different rhizobia, no consolidated models have been formulated to describe the central physiologic changes that occur in acid-stressed bacteria. We present here an integrated analysis entailing the main cultural, metabolic, and molecular responses of the model bacterium Sinorhizobium meliloti growing under controlled acid stress in a chemostat. A stepwise extracellular acidification of the culture medium had indicated that S. meliloti stopped growing at ca. pH 6.0-6.1. Under such stress the rhizobia increased the O-2 consumption per cell by more than 5-fold. This phenotype, together with an increase in the transcripts for several membrane cytochromes, entails a higher aerobic-respiration rate in the acid-stressed rhizobia. Multivariate analysis of global metabolome data served to unequivocally correlate specific-metabolite profiles with the extracellular pH, showing that at low pH the pentose-phosphate pathway exhibited increases in several transcripts, enzymes, and metabolites. Further analyses should be focused on the time course of the observed changes, its associated intracellular signaling, and on the comparison with the changes that operate during the sub lethal acid-adaptive response (ATR) in rhizobia.
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Draghi WO, Del Papa MF, Hellweg C, et al. A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti. SCIENTIFIC REPORTS. 2016;6(1): 29278.
Draghi, W. O., Del Papa, M. F., Hellweg, C., Watt, S. A., Watt, T. F., Barsch, A., Lozano, M. J., et al. (2016). A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti. SCIENTIFIC REPORTS, 6(1), 29278. doi:10.1038/srep29278
Draghi, W. O., Del Papa, M. F., Hellweg, C., Watt, S. A., Watt, T. F., Barsch, A., Lozano, M. J., Lagares, A., J., Salas, M. E., Lopez, J. L., et al. (2016). A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti. SCIENTIFIC REPORTS 6:29278.
Draghi, W.O., et al., 2016. A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti. SCIENTIFIC REPORTS, 6(1): 29278.
W.O. Draghi, et al., “A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti”, SCIENTIFIC REPORTS, vol. 6, 2016, : 29278.
Draghi, W.O., Del Papa, M.F., Hellweg, C., Watt, S.A., Watt, T.F., Barsch, A., Lozano, M.J., Lagares, A., J., Salas, M.E., Lopez, J.L., Albicoro, F.J., Nilsson, J.F., Torres Tejerizo, G.A., Luna, M.F., Pistorio, M., Boiardi, J.L., Pühler, A., Weidner, S., Niehaus, K., Lagares, A.: A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti. SCIENTIFIC REPORTS. 6, : 29278 (2016).
Draghi, W. O., Del Papa, M. F., Hellweg, C., Watt, S. A., Watt, T. F., Barsch, A., Lozano, M. J., Lagares, A., Jr., Salas, M. E., Lopez, J. L., Albicoro, F. J., Nilsson, J. F., Torres Tejerizo, G. A., Luna, M. F., Pistorio, M., Boiardi, J. L., Pühler, Alfred, Weidner, Stefan, Niehaus, Karsten, and Lagares, A. “A consolidated analysis of the physiologic and molecular responses induced under acid stress in the legume-symbiont model-soil bacterium Sinorhizobium meliloti”. SCIENTIFIC REPORTS 6.1 (2016): 29278.

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Bustamante-Brito R, Vera-Ponce de León A, Rosenblueth M, Martínez-Romero JC, Martínez-Romero E., Life (Basel) 9(1), 2019
PMID: 30609847
Common dyes used to determine bacterial polysaccharides on agar are affected by medium acidification.
Hawkins JP, Geddes BA, Oresnik IJ., Can J Microbiol 63(6), 2017
PMID: 28253454
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da-Silva JR, Alexandre A, Brígido C, Oliveira S., AIMS Microbiol 3(3), 2017
PMID: 31294167

103 References

Daten bereitgestellt von Europe PubMed Central.

Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature.
Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C., J. Bacteriol. 185(24), 2003
PMID: 14645288
Genomes of the symbiotic nitrogen-fixing bacteria of legumes.
MacLean AM, Finan TM, Sadowsky MJ., Plant Physiol. 144(2), 2007
PMID: 17556525
Biology of the Parasponia-Bradyrhizobium symbiosis

The role of nitrogen fixation in crop production.
O'Hara GW., Journal of crop production. 1(2), 1998
PMID: IND21981102
Nitrogen fixation in perspective: an overview of research and extension needs
Biotechnological solutions to the nitrogen problem.
Oldroyd GE, Dixon R., Curr. Opin. Biotechnol. 26(), 2013
PMID: 24679253
Acid tolerance in root nodule bacteria.
Glenn AR, Reeve WG, Tiwari RP, Dilworth MJ., Novartis Found. Symp. 221(), 1999
PMID: 10207916
Global extent, development and economic impact of acid soils
Acid-tolerance in the Rhizobium meliloti-Medicago symbiosis
Acid-tolerant species of Medicago produce root exudates at low pH which induce the expression of nodulation genes in Rhizobium meliloti
Survival of Rhizobium in Acid soils.
Lowendorf HS, Baya AM, Alexander M., Appl. Environ. Microbiol. 42(6), 1981
PMID: 16345909
Adsorption of Rhizobium meliloti to alfalfa roots: Dependence on divalent cations and pH
Nodulation of Medicago sativa in solution culture
Effects of soil acidity on rhizobia numbers, nodulation and nitrogen fixation by alfalfa and red clover
Cultivar and pH effects on competition for nodule sites between isolates of Rhizobium in beans
Effect of low pH on nitrogen fixation of common bean grown at various calcium and nitrate levels
Low pH changes the profile of nodulation factors produced by Rhizobium tropici CIAT899.
Moron B, Soria-Diaz ME, Ault J, Verroios G, Noreen S, Rodriguez-Navarro DN, Gil-Serrano A, Thomas-Oates J, Megias M, Sousa C., Chem. Biol. 12(9), 2005
PMID: 16183027
Expression of Nodulation Genes in Rhizobium leguminosarum biovar trifolii Is Affected by Low pH and by Ca and Al Ions.
Richardson AE, Simpson RJ, Djordjevic MA, Rolfe BG., Appl. Environ. Microbiol. 54(10), 1988
PMID: 16347761
Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil condition
Calcium affects the growth and survival of Rhizobium meliloti.
Reeve WG, Tiwari RP, Dilworth MJ, Glenn AR., Soil Biol. Biochem. 25(5), 1993
PMID: IND93050450
Isolation and characterization of alfalfa-nodulating rhizobia present in acidic soils of central argentina and uruguay
del Papa MF , Balague LJ, Sowinski SC, Wegener C, Segundo E, Abarca FM, Toro N, Niehaus K, P hler A , Aguilar OM, Martinez-Drets G, Lagares A., Appl. Environ. Microbiol. 65(4), 1999
PMID: 10103231
Selection for acid tolerance in Rhizobium meliloti
A microcosm study on the influence of pH and the host-plant on the soil persistence of two alfalfa-nodulating rhizobia with different saprophytic and symbiotic characteristics
Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899
Acid-tolerance and symbiotic effectiveness of Rhizobium trifolii associated with a Trifolium subterraneum L.-based pasture growing in an acid soil
Characterisation of symbiotically efficient alfalfa-nodulating rhizobia isolated from acid soils of Argentina and Uruguay
Saprophytic competence of acid tolerant strains of Rhizobium trifolii in acid soil
An essential role for actA in acid tolerance of Rhizobium meliloti.
Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR., Microbiology (Reading, Engl.) 142 ( Pt 3)(), 1996
PMID: 8868435
Acid tolerance in Rhizobium meliloti strain WSM419 involves a two-component sensor-regulator system.
Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR., Microbiology (Reading, Engl.) 142 ( Pt 7)(), 1996
PMID: 8757734
Sinorhizobium medicae genes whose regulation involves the ActS and/or ActR signal transduction proteins.
Fenner BJ, Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR., FEMS Microbiol. Lett. 236(1), 2004
PMID: 15212786

The transcriptional regulator gene phrR in Sinorhizobium meliloti WSM419 is regulated by low pH and other stresses.
Reeve WG, Tiwari RP, Wong CM, Dilworth MJ, Glenn AR., Microbiology (Reading, Engl.) 144 ( Pt 12)(), 1998
PMID: 9884225
Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness.
Vinuesa P, Neumann-Silkow F, Pacios-Bras C, Spaink HP, Martinez-Romero E, Werner D., Mol. Plant Microbe Interact. 16(2), 2003
PMID: 12575750
The Sinorhizobium medicae WSM419 lpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions.
Reeve WG, Brau L, Castelli J, Garau G, Sohlenkamp C, Geiger O, Dilworth MJ, Glenn AR, Howieson JG, Tiwari RP., Microbiology (Reading, Engl.) 152(Pt 10), 2006
PMID: 17005985
Adaptive acidification tolerance response of Salmonella typhimurium.
Foster JW, Hall HK., J. Bacteriol. 172(2), 1990
PMID: 2404956
Resistance of acid-habituated Escherichia coli to organic acids and its medical and applied significance
Survival and exopolysaccharide production in Sinorhizobium meliloti WSM419 are affected by calcium and low pH.
Dilworth MJ, Rynne FG, Castelli JM, Vivas-Marfisi AI, Glenn AR., Microbiology (Reading, Engl.) 145 ( Pt 7)(), 1999
PMID: 10439397
Cultural conditions required for the induction of an adaptive acid-tolerance response (ATR) in Sinorhizobium meliloti and the question as to whether or not the ATR helps rhizobia improve their symbiosis with alfalfa at low pH.
Draghi WO, Del Papa MF, Pistorio M, Lozano M, de Los Angeles Giusti M, Torres Tejerizo GA, Jofre E, Boiardi JL, Lagares A., FEMS Microbiol. Lett. 302(2), 2009
PMID: 19958387
The adaptive acid tolerance response in root nodule bacteria and Escherichia coli.
O'Hara GW, Glenn AR., Arch. Microbiol. 161(4), 1994
PMID: 8002711
Probing for pH-regulated proteins in Sinorhizobium medicae using proteomic analysis.
Reeve WG, Tiwari RP, Guerreiro N, Stubbs J, Dilworth MJ, Glenn AR, Rolfe BG, Djordjevic MA, Howieson JG., J. Mol. Microbiol. Biotechnol. 7(3), 2004
PMID: 15263818
Continuous culture--making a comeback?
Hoskisson PA, Hobbs G., Microbiology (Reading, Engl.) 151(Pt 10), 2005
PMID: 16207900
Maintenance of Intracellular pH and Acid Tolerance in Rhizobium meliloti.
O'hara GW, Goss TJ, Dilworth MJ, Glenn AR., Appl. Environ. Microbiol. 55(8), 1989
PMID: 16347984
The composite genome of the legume symbiont Sinorhizobium meliloti.
Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, Bothe G, Boutry M, Bowser L, Buhrmester J, Cadieu E, Capela D, Chain P, Cowie A, Davis RW, Dreano S, Federspiel NA, Fisher RF, Gloux S, Godrie T, Goffeau A, Golding B, Gouzy J, Gurjal M, Hernandez-Lucas I, Hong A, Huizar L, Hyman RW, Jones T, Kahn D, Kahn ML, Kalman S, Keating DH, Kiss E, Komp C, Lelaure V, Masuy D, Palm C, Peck MC, Pohl TM, Portetelle D, Purnelle B, Ramsperger U, Surzycki R, Thebault P, Vandenbol M, Vorholter FJ, Weidner S, Wells DH, Wong K, Yeh KC, Batut J., Science 293(5530), 2001
PMID: 11474104
A global analysis of protein expression profiles in Sinorhizobium meliloti: discovery of new genes for nodule occupancy and stress adaptation.
Djordjevic MA, Chen HC, Natera S, Van Noorden G, Menzel C, Taylor S, Renard C, Geiger O, Weiller GF; Sinorhizobium DNA Sequencing Consortium., Mol. Plant Microbe Interact. 16(6), 2003
PMID: 12795377
Trigger Factor and DnaK possess overlapping substrate pools and binding specificities.
Deuerling E, Patzelt H, Vorderwulbecke S, Rauch T, Kramer G, Schaffitzel E, Mogk A, Schulze-Specking A, Langen H, Bukau B., Mol. Microbiol. 47(5), 2003
PMID: 12603737
Visualization of elongation factor Tu on the Escherichia coli ribosome.
Stark H, Rodnina MV, Rinke-Appel J, Brimacombe R, Wintermeyer W, van Heel M., Nature 389(6649), 1997
PMID: 9311785
Recent advances in peptide chain termination.
Craigen WJ, Lee CC, Caskey CT., Mol. Microbiol. 4(6), 1990
PMID: 2215213
Translational control of the cytosolic stress response by mitochondrial ribosomal protein L18.
Zhang X, Gao X, Coots RA, Conn CS, Liu B, Qian SB., Nat. Struct. Mol. Biol. 22(5), 2015
PMID: 25866880
Families of serine peptidases.
Rawlings ND, Barrett AJ., Meth. Enzymol. 244(), 1994
PMID: 7845208
Genetic analysis of polynucleotide phosphorylase structure and functions.
Briani F, Del Favero M, Capizzuto R, Consonni C, Zangrossi S, Greco C, De Gioia L, Tortora P, Deho G., Biochimie 89(1), 2006
PMID: 17084501
Lysis genes of the Bacillus subtilis defective prophage PBSX.
Krogh S, Jorgensen ST, Devine KM., J. Bacteriol. 180(8), 1998
PMID: 9555893
A Sinorhizobium meliloti osmosensory two-component system required for cyclic glucan export and symbiosis.
Griffitts JS, Carlyon RE, Erickson JH, Moulton JL, Barnett MJ, Toman CJ, Long SR., Mol. Microbiol. 69(2), 2008
PMID: 18630344
Antagonistic Roles for GcvA and GcvB in hdeAB Expression in Escherichia coli.
Stauffer LT, Stauffer GV., ISRN Microbiol 2012(), 2012
PMID: 23762759
Identification of a gene required for the biosynthesis of ornithine-derived lipids.
Weissenmayer B, Gao JL, Lopez-Lara IM, Geiger O., Mol. Microbiol. 45(3), 2002
PMID: 12139618
Bacterial membrane lipids: diversity in structures and pathways.
Sohlenkamp C, Geiger O., FEMS Microbiol. Rev. 40(1), 2015
PMID: 25862689
Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid.
Barnett MJ, Fisher RF, Jones T, Komp C, Abola AP, Barloy-Hubler F, Bowser L, Capela D, Galibert F, Gouzy J, Gurjal M, Hong A, Huizar L, Hyman RW, Kahn D, Kahn ML, Kalman S, Keating DH, Palm C, Peck MC, Surzycki R, Wells DH, Yeh KC, Davis RW, Federspiel NA, Long SR., Proc. Natl. Acad. Sci. U.S.A. 98(17), 2001
PMID: 11481432
Probing for pH-regulated genes in Sinorhizobium medicae using transcriptional analysis.
Tiwari RP, Reeve WG, Fenner BJ, Dilworth MJ, Glenn AR, Howieson JG., J. Mol. Microbiol. Biotechnol. 7(3), 2004
PMID: 15263817
Respiration of Escherichia coli can be fully uncoupled via the nonelectrogenic terminal cytochrome bd-II oxidase.
Bekker M, de Vries S, Ter Beek A, Hellingwerf KJ, de Mattos MJ., J. Bacteriol. 191(17), 2009
PMID: 19542282
Cyclic organization of the carbohydrate metabolism in Sinorhizobium meliloti.
Portais JC, Tavernier P, Gosselin I, Barbotin JN., Eur. J. Biochem. 265(1), 1999
PMID: 10491206
Observations on the carbohydrate metabolism of tumours.
Crabtree HG., Biochem. J. 23(3), 1929
PMID: 16744238
Pyruvate metabolism in Saccharomyces cerevisiae.
Pronk JT, Yde Steensma H, Van Dijken JP., Yeast 12(16), 1996
PMID: 9123965
Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms.
Paczia N, Nilgen A, Lehmann T, Gatgens J, Wiechert W, Noack S., Microb. Cell Fact. 11(), 2012
PMID: 22963408
The acetate switch.
Wolfe AJ., Microbiol. Mol. Biol. Rev. 69(1), 2005
PMID: 15755952

Peribacteroid space acidification: a marker of mature bacteroid functioning in Medicago truncatula nodules.
Pierre O, Engler G, Hopkins J, Brau F, Boncompagni E, Herouart D., Plant Cell Environ. 36(11), 2013
PMID: 23586685
An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing.
Roux B, Rodde N, Jardinaud MF, Timmers T, Sauviac L, Cottret L, Carrere S, Sallet E, Courcelle E, Moreau S, Debelle F, Capela D, de Carvalho-Niebel F, Gouzy J, Bruand C, Gamas P., Plant J. 77(6), 2014
PMID: 24483147
The continuous cultivation of micro-organisms. II. Construction of a chemostat
Computer-aided material balancing for prediction of fermentation parameters.
Cooney CL, Wang HY, Wang DI., Biotechnol. Bioeng. 19(1), 1977
PMID: 321044
Determination of ammonia in natural waters by the phenolhypochlorite method
Determination of yeast carbohydrates with the anthrone reagent.
TREVELYAN WE, FORREST RS, HARRISON JS., Nature 170(4328), 1952
PMID: 13002392
Assay of poly-beta-hydroxybutyric acid.
LAW JH, SLEPECKY RA., J. Bacteriol. 82(), 1961
PMID: 13759651
Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions.
Becker A, Berges H, Krol E, Bruand C, Ruberg S, Capela D, Lauber E, Meilhoc E, Ampe F, de Bruijn FJ, Fourment J, Francez-Charlot A, Kahn D, Kuster H, Liebe C, Puhler A, Weidner S, Batut J., Mol. Plant Microbe Interact. 17(3), 2004
PMID: 15000396
Exploring the metabolic and genetic control of gene expression on a genomic scale.
DeRisi JL, Iyer VR, Brown PO., Science 278(5338), 1997
PMID: 9381177
Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression.
Ruberg S, Tian ZX, Krol E, Linke B, Meyer F, Wang Y, Puhler A, Weidner S, Becker A., J. Biotechnol. 106(2-3), 2003
PMID: 14651866
Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation.
Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP., Nucleic Acids Res. 30(4), 2002
PMID: 11842121
EMMA: a platform for consistent storage and efficient analysis of microarray data.
Dondrup M, Goesmann A, Bartels D, Kalinowski J, Krause L, Linke B, Rupp O, Sczyrba A, Puhler A, Meyer F., J. Biotechnol. 106(2-3), 2003
PMID: 14651856
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository.
Edgar R, Domrachev M, Lash AE., Nucleic Acids Res. 30(1), 2002
PMID: 11752295
Comprehensive metabolite profiling of Sinorhizobium meliloti using gas chromatography-mass spectrometry.
Barsch A, Patschkowski T, Niehaus K., Funct. Integr. Genomics 4(4), 2004
PMID: 15372312
MetaboAnalyst 2.0--a comprehensive server for metabolomic data analysis.
Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS., Nucleic Acids Res. 40(Web Server issue), 2012
PMID: 22553367
The COG database: an updated version includes eukaryotes.
Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA., BMC Bioinformatics 4(), 2003
PMID: 12969510


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