Abstract
An increasing number of studies have demonstrated that arbuscular mycorrhizal fungi can cooperate with other soil microorganisms, e.g., bacteria, which develop near or on the surface of the extraradical hyphae where they perform multiple functions. However, the mechanisms involved in this privileged relationship are still poorly known. In the present study, we investigated how the arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 43194 influences the three pace-making enzymes (i.e., citrate synthase, isocitrate dehydrogenase, and α-oxoglutarate dehydrogenase) of the tricarboxylic acid (TCA) cycle in the phosphate-solubilizing bacterium Rahnella aquatilis HX2. The study was conducted under strict in vitro culture conditions and analysis made at the transcriptional level. Results showed that R. irregularis induced the expression of the gene-encoding citrate synthase (gltA), the pace-making enzyme involved in the first step of the TCA cycle, in R. aquatilis at all time points of observation (i.e., 1, 6, 12, 24, 48, and 72 h). The expression of the gene-encoding isocitrate dehydrogenase (icd) significantly decreased at 6, 12, 24, 48, and 72 h and the expression of the gene-encoding α-oxoglutarate dehydrogenase E1 component (kgdhc) significantly increased at 1, 6, and 48 h. The above results suggested that R. irregularis may influence the level of adenosine triphosphate production in R. aquatilis and thus the metabolism of the bacterium by stimulating the expression of gltA involved in the TCA cycle. Our results suggest a fine-tuned dialog between R. irregularis MUCL 43194 and R. aquatilis HX2 and emphasize the complexity of the interactions that might take place at the hyphal surface of arbuscular mycorrhizal fungi hosting communities of microbes.
References
Agnolucci M, Battini F, Cristani C, Giovannetti M (2015) Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biol Fertil Soils 51:379–389
Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10
Bender SF, Plantenga F, Neftel A, Jocher M, Oberholzer HR, Köhl L, Giles M, Daniell TJ, van der Heijden M (2014) Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. ISME J 8:1336–1345
Bharadwaj DP, Alstrom S, Lundquist P-O (2012) Interactions among Glomus irregulare, arbuscular mycorrhizal spore-associated bacteria, and plant pathogens under in vitro conditions. Mycorrhiza 22:437–447
Chao G, Shen J, Tseng CP, Park SJ, Gunsalus RP (1997) Aerobic regulation of isocitrate dehydrogenase gene (icd) expression in Escherichia coli by the arcA and fnr gene products. J Bacteriol 179:4299–4304
Chavarría M, Durante-Rodriguez G, Krell T, Santiago C, Brezovsky J, Damborsky J, de Lorenzo V (2014) Fructose 1-phosphate is the one and only physiological effector of the Cra (FruR) regulator of Pseudomonas putida. FEBS Open Bio 4:377–386
Chen F, Guo YB, Wang JH, Li JY, Wang HM (2007) Biological control of grape crown gall by Rahnella aquatilis HX2. Plant Dis 91:957–963
Declerck S, Strullu DG, Plenchette C (1998) Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90:579–585
Declerck S, Dupré de Boulois H, Bivort C, Delvaux B (2003) Extraradical mycelium of the arbuscular mycorrhizal fungus Glomus lamellosum can take up, accumulate and translocate radiocaesium under root-organ culture conditions. Environ Microbiol 5:510–516
Domínguez-Martín MA, López-Lozano A, Rangel-Zúñiga OA, Díez J, García-Fernández JM (2018) Distinct features of C/N balance regulation in Prochlorococcus sp. strain MIT9313. FEMS Microbiol Lett 365:fnx278
Erfle JD, Sauer F (1969) The inhibitory effects of acyl-coenzyme a esters on the pyruvate and α-oxoglutarate dehydrogenase complexes. BBA-Enzymology 178:441–452
Guo YB, Li JY, Li L, Chen F, Wu WL, Wang JH, Wang HM (2009) Mutations that disrupt either the pqq or the gdh gene of Rahnella aquatilis abolish the production of an antibacterial substance and result in reduced biological control of grapevine crown gall. Appl Environ Microbiol 75:6792–6803
Guo Y, Jiao Z, Li L, Wu D, Crowley DE, Wang Y, Wu W (2012) Draft genome sequence of Rahnella aquatilis strain HX2, a plant growth-promoting rhizobacterium isolated from vineyard soil in Beijing, China. J Bacteriol 194:6646–6647
Holmes DE, Nevin KP, O'Neil RA, Ward JE, Adams LA, Woodard TL, Vrionis HA, Lovley DR (2005) Potential for quantifying expression of the Geobacteraceae citrate synthase gene to assess the activity of Geobacteraceae in the subsurface and on current-harvesting electrodes. Appl Environ Microbiol 71:6870–6877
Iffis B, St-Arnaud M, Hijri M (2016) Petroleum hydrocarbon contamination, plant identity and arbuscular mycorrhizal fungal (AMF) community determine assemblages of the AMF spore-associated microbes. Environ Microbiol 18:2689–2704
Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy D (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205:1537–1551
Karasawa T, Hodge A, Fitter AH (2012) Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil. Plant Cell Environ 35:819–828
Korkes S, Del Campillo A, Gunsalas IC, Ochoa S (1951) Enzymatic synthesis of citric acid. IV. Pyruvate as acetyl donor. J Biol Chem 193:721–735
Krebs HA (1970) Rate control of the tricarboxylic acid cycle. Adv Enzym Regul 8:335–353
Leigh J, Fitter AH, Hodge A (2011) Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiol Ecol 76:428–438
Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15:1870–1881
Peng B, Su Y, Li H, Han Y, Guo C, Tian Y, Peng X (2015) Exogenous alanine and/or glucose plus kanamycin kills antibiotic-resistant bacteria. Cell Metab 21:249–262
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921
Ririe KM, Rasmussen RP, Wittwer CT (1997) Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 245:154–160
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York
Storer K, Coggan A, Ineson P, Hodge A (2017) Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol. https://doi.org/10.1111/nph.14931
Tajadini M, Panjehpour M, Javanmard SH (2014) Comparison of SYBR green and TaqMan methods in quantitative real-time polymerase chain reaction analysis of four adenosine receptor subtypes. Adv Biomed Res 3:85
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Becard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JPW, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110:20117–20122
Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304
Tortora GJ, Funke BR, Case CL (2016) Microbiology: an introduction, 12th edn. Pearson Education, USA
Utter MF, Keech DB (1960) Formation of oxaloacetate from pyruvate and CO2. J Biol Chem 235:PC17–PC18
Wang F, Shi N, Jiang R, Zhang F, Feng G (2016) In situ stable isotope probing of phosphate-solubilizing bacteria in the hyphosphere. J Exp Bot 67:1689–1701
Webb M (1964) The biological action of cobalt and other metals: IV. Inhibition of α-oxoglutarate dehydrogenase. BBA – Specialized Section on Enzymological Subjects 89:431–446
Zhang L, Fan J, Ding X, He X, Zhang F, Feng G (2014) Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. Soil Biol Biochem 74:177–183
Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032
Zhang L, Feng G, Declerck S (2018) Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. ISME J 12:2339–2351
Acknowledgments
We further thank the China Scholarship Council (File No. 201306350121) for providing a scholarship to Lin Zhang.
Funding
This study is financially supported by the National Natural Science Foundation of China (31701998, U1703232).
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Zhang, L., Fan, J., Feng, G. et al. The arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 43194 induces the gene expression of citrate synthase in the tricarboxylic acid cycle of the phosphate-solubilizing bacterium Rahnella aquatilis HX2. Mycorrhiza 29, 69–75 (2019). https://doi.org/10.1007/s00572-018-0871-7
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DOI: https://doi.org/10.1007/s00572-018-0871-7