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Evaluation of growth and motility in non-photosynthetic Azospirillum brasilense exposed to red, blue, and white light

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Abstract

Azospirillum brasilense is a non-photosynthetic rhizobacterium that promotes the growth of plants. In this work, we evaluated the effects of different light qualities on the growth, viability, and motility in combination to other culture conditions such as temperature or composition of the culture medium. Exponential cultures of A. brasilense Az39 were inoculated by drop-plate method on nutritionally rich (LB) or chemically defined (MMAB) media in the presence or absence of Congo Red indicator (CR) and exposed continuously to white light (WL), blue light (BL), and red light (RL), or maintained in dark conditions (control). The exposure to BL or WL inhibited growth, mostly in LB medium at 36 °C. By contrast, the exposure to RL showed a similar behavior to the control. Swimming motility was inhibited by exposure to WL and BL, while exposure to RL caused only a slight reduction. The effects of WL and BL on plant growth-promoting rhizobacteria should be considered in the future as deleterious factors that could be manipulated to improve the functionality of foliar inoculants, as well as the bacterial effects on the leaf after inoculation.

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  • 17 June 2020

    In the original article, last name and first names of all the authors are inverted. The correct names should appears as ���Romina Molina, Gast��n L��pez, Bel��n Rodr��guez, Susana Rosas, Ver��nica Mora, Fabricio Cass��n���.

References

  • Alexandre G (2015) Minireview: chemotaxis control of transient cell aggregation. J Bacteriol 197(20):3230–3237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amin RM, Bhayana B, Hamblin MR, Dai T (2016) Antimicrobial blue light inactivation of Pseudomonas aeruginosa by photo-excitation of endogenous porphyrins: in vitro and in vivo studies. Lasers Surg Med 48(5):562–568

    Article  PubMed  PubMed Central  Google Scholar 

  • Armitage JP, Hellingwerf KJ (2005) Light-induced behavioral responses (‘phototaxis’) in prokaryotes. Discoveries in photosynthesis. Springer, Dordrecht, Berlin, pp 985–995

    Google Scholar 

  • Ashkenazi H, Malik Z, Harth Y, Nitzan Y (2003) Eradication of Propionibacterium acnes by its endogenic porphyrins after illumination with high intensity blue light. FEMS Immunol Med Microbiol 35:17–24

    Article  CAS  PubMed  Google Scholar 

  • Atkinson S, Chang CY, Sockett RE, Cámara M, Williams P (2006) Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J Bacteriol 188(4):1451–1461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldani VLD, Baldani JI, Olivares F, Döbereiner J (1992) Identification and ecology of Herbaspirillum seropedicae and the closely related Pseudomonas rubrisubalbicans. Symbiosis Rehovot 12:65

    Google Scholar 

  • Bertani G (1951) Studies on lysogenesis I.: the mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62(3):293–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bible AN, Khalsa-Moyers GK, Mukherjee T, Green CS, Mishra P, Purcell A, Alexandre G (2015) Metabolic adaptations of Azospirillum brasilense to oxygen stress by cell-cell clum** and flocculation. Appl Environ Microbiol 81:8346–8357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budanova AA, Shirokov AA, Shchyogolev SY, Matora LY (2018) Analysis of Congo red-induced changes in the cell surface and macrocolony structure of the bacterium Azospirillum brasilense. Microbiology 87(1):60–65

    Article  CAS  Google Scholar 

  • Cassán F, Diaz-Zorita M (2016) Azospirillum sp. in current agriculture: from the laboratory to the field. Soil Biol Biochem 103:117–130

    Article  CAS  Google Scholar 

  • Christie JM, Salomon M, Nozue K, Wada M, Briggs WR (1999) LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc Natl Acad Sci USA 96:8779–8783

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Saez Y, Díaz-de los Ríos M, Alberto-Casas M, Nuñez-Caraballo A, Martínez-Mora M (2013) Crecimiento de Azospirillum brasilense en presencia de disacáridos: sacarosa y lactosa. ICIDCA. Sobre los Derivados de la Caña de Azúcar 47(2)

  • Dimitrova R, Mironova R, Ivanov I (2004) Glycation of proteins in Escherichia coli: effect of nutrient broth ingredients on glycation. Biotechnol Biotechnol Equip 18:99–103

    Article  CAS  Google Scholar 

  • Elías-Arnanz M, Padmanabhan S, Murillo FJ (2011) Light-dependent gene regulation in nonphototrophic bacteria. Curr Opin Microbiol 14:128–135

    Article  PubMed  CAS  Google Scholar 

  • Feuerstein O, Persman N, Weiss EI (2004) Phototoxic effect of visible light on Porphyromonas gingivalis and Fusobacterium nucleatum: an in vitro study. Photochem Photobiol 80:412–415

    Article  CAS  PubMed  Google Scholar 

  • Foreman R, Fiebig A, Crosson S (2012) The LovK-LovR two-component system is a regulator of the general stress pathway in Caulobacter crescentus. J Bacteriol 194(12):3038–3049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukami J, Nogueira MA, Araujo RS, Hungria M (2016) Accessing inoculation methods of maize and wheat with Azospirillum brasilense. AMB Express 6(1):3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fukami J, de la Osa C, Ollero FJ, Megías M, Hungria M (2018) Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress. Funct Plant Biol 45(3):328–339

    Article  CAS  PubMed  Google Scholar 

  • Gest H (1995) Phototaxis and other sensory phenomena in purple photosynthetic bacteria. FEMS Microbiol Rev 16:287–294

    Article  CAS  Google Scholar 

  • Grishanin RN, Chalmina II, Zhulin IB (1991) Behaviour of Azospirillum brasilense in a spatial gradient of oxygen an in a ‘redox’ gradient of an artificial electron acceptor. J Gen Microbiol 137:2781–2785

    Article  CAS  Google Scholar 

  • Guffey JS, Wilborn J (2006) In vitro bactericidal effects of 405-nm and 470-nm blue light. Photomed Laser Surg 24:684–688

    Article  PubMed  Google Scholar 

  • Häder DP (1987) Photosensory behavior in procaryotes. Microbiol Rev 51(1):1

    Article  PubMed  PubMed Central  Google Scholar 

  • Hessling M, Spellerberg B, Hoenes K (2017) Photoinactivation of bacteria by endogenous photosensitizers and exposure to visible light of different wavelengths—a review on existing data. FEMS Microbiol Lett 364(2):fnw270

    Article  PubMed  CAS  Google Scholar 

  • Hitomi K, Okamoto K, Daiyasu H, Miyashita H, Iwai S, Toh H, Todo T (2000) Bacterial cryptochrome and photolyase: characterization of two photolyase-like genes of Synechocystis sp. PCC6803. Nucleic Acids Res 28(12):2353–2362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James EK, Reis VM, Olivares FL, Baldani JI, Döbereiner J (1994) Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J Exp Bot 6(1):757–766

    Article  Google Scholar 

  • Jiang ZY, Rushing BG, Bai Y, Gest H, Bauer CE (1998) Isolation of Rhodospirillum centenum mutants defective in phototactic colony motility by transposon mutagenesis. J Bacteriol 180:1248–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaushik R, Saxena A, Tilak KVBR (2002) Can Azospirillum strains capable of growing at a sub-optimal temperature perform better in field-grown-wheat rhizosphere. Biol Fert Soils 35(2):92–95

    Article  Google Scholar 

  • Konnova SA, Makarov OE, Skvortsov IM, Ignatov VV (1994) Isolation, fractionation and some properties of polysaccharides produced in a bound form by Azospirillum brasilense and their possible involvement in Azospirillum-wheat root interactions. FEMS Microbiol Lett 118(1–2):93–99

    Article  CAS  Google Scholar 

  • Kram KE, Finkel SE (2015) Rich medium composition affects Escherichia coli survival, glycation, and mutation frequency during long-term batch culture. Appl Environ Microbiol 81:4442–4450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Kateriya S, Singh VS, Tanwar M, Agarwal S, Singh H, Tripathi AK (2012) Bacteriophytochrome controls carotenoid-independent response to photodynamic stress in a non-photosynthetic rhizobacterium, Azospirillum brasilense Sp7. Sci Rep 2:1

    Google Scholar 

  • Lubart R, Lipovski A, Nitzan Y, Friedmann H (2011) A possible mechanism for the bactericidal effect of visible light. Laser Therapy 20(1):17–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maclean M, MacGregor SJ, Anderson JG, Woolsey G (2008) High-intensity narrow-spectrum light inactivation and wavelength sensitivity of Staphylococcus aureus. FEMS Microbiol Lett 285:227–232

    Article  CAS  PubMed  Google Scholar 

  • Michiels KW, Croes CL, Vanderleyden J (1991) Two different modes of attachment of Azospirillum brasilense Sp7 to wheat roots. Microbiology 137(9):2241–2246

    CAS  Google Scholar 

  • Miles A, Misra S (1938) The estimation of the bactericidal power of blood. J Hyg 38(06):732–737

    CAS  PubMed  Google Scholar 

  • Mironova R, Niwa T, Hayashi H, Dimitrova R, Ivanov I (2001) Evidence for non-enzymatic glycosylation in Escherichia coli. Mol Microbiol 39:1061–1068

    Article  CAS  PubMed  Google Scholar 

  • Molina R, Obando D, Torres D, Rivera D, Cassán F (2014) Utilización de un medio de cultivo para la cuantificación y la diferenciación de bacterias presentes en la misma formulación. Libro de resúmenes digital, pp 249

  • Oberpichler I, Rosen R, Rasouly A, Vugman M, Ron EZ, Lamparter T (2008) Light affects motility and infectivity of Agrobacterium tumefaciens. Environ Microbiol 10(8):2020–2029

    Article  CAS  PubMed  Google Scholar 

  • Preininger C, Sauer U, Bejarano A, Berninger T (2018) Concepts and applications of foliar spray for microbial inoculants. App Microbiol Biotechnol 102(17):7265–7282

    Article  CAS  Google Scholar 

  • Puente ML, Gualpa JL, Lopez GA, Molina RM, Carletti SM, Cassán FD (2017) The benefits of foliar inoculation with Azospirillum brasilense in soybean are explained by an auxin signaling model. Symbiosis 76:41–49

    Article  CAS  Google Scholar 

  • Puente ML, Zawoznik M, de Sabando ML, Perez G, Gualpa JL, Carletti SM, Cassán FD (2018) Improvement of soybean grain nutritional quality under foliar inoculation with Azospirillum brasilense strain Az39. Symbiosis 77:41–47

    Article  CAS  Google Scholar 

  • Purcell EB, Siegal-Gaskins D, Rawling DC, Fiebig A, Crosson S (2007) A photosensory two-component system regulates bacterial cell attachment. Proc Natl Acad Sci USA 104(46):18241–18246

    Article  CAS  PubMed  Google Scholar 

  • Ragatz L, Jiang ZY, Bauer CE, Gest H (1995) Macroscopic phototactic behavior of the purple photosyn thetic bacterium Rhodospirillum centenum. Arch Microbiol 163:1–6

    Article  CAS  PubMed  Google Scholar 

  • Ramos HC, Rumbo M, Sirard JC (2004) Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12:509–517

    Article  CAS  PubMed  Google Scholar 

  • Rivera D, Revale S, Molina R, Gualpa J, Puente M, Maroniche G, Spaepen S (2014) Complete genome sequence of the model rhizosphere strain Azospirillum brasilense Az39, successfully applied in agriculture. Genome announc 2(4):e00683-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Sinha RP, Hader DP (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236

    Article  CAS  PubMed  Google Scholar 

  • Souza R, Meyer J, Schoenfeld R, Costa PB, Passaglia LMP (2014) Characterization of plant growth-promoting bacteria associated with rice cropped in iron-stressed soils. Ann Microbiol 65:951–964

    Article  CAS  Google Scholar 

  • Takano H, Obitsu S, Beppu T, Ueda K (2005) Light-induced carotenogenesis in Streptomyces coelicolor A3 (2): identification of an extracytoplasmic function sigma factor that directs photodependent transcription of the carotenoid biosynthesis gene cluster. J Bacteriol 187(5):1825–1832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulrich LE, Koonin EV, Zhulin IB (2005) One-component systems dominate signal transduction in prokaryotes. Trends Microbiol 13:52–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Horst MA, Hellingwerf KJ (2004) Photoreceptor proteins, “star actors of modern times”: a review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc Chem Res 37(1):13–20

    Article  PubMed  CAS  Google Scholar 

  • Vanstockem M, Michiels K, Vanderleyden J, Van Gool AP (1987) Transposon mutagenesis of Azospirillum brasilense and Azospirillum lipoferum: physical analysis of Tn5 and Tn5-Mob insertion mutants. Appl Environ Microbiol 53(2):410–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilde A, Mullineaux CW (2017) Light-controlled motility in prokaryotes and the problem of directional light perception. FEMS Microbiol Rev 41(6):900–922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, McGrane RS, Beattie GA (2013) Light regulation of swarming motility in Pseudomonas syringae integrates signaling pathways mediated by a bacteriophytochrome and a LOV protein. MBio 4(3):e00334-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wuichet K, Cantwell BJ, Zhulin IB (2010) Evolution and phyletic distribution of two-component signal transduction systems. Curr Opin Microbiol 13:219–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziegelhoffer EC, Donohue TJ (2009) Bacterial responses to photo-oxidative stress. Nat Rev Microbiol 7:856–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding was provided by FONCyT (Grant No. PICT-2015-1599).

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Correspondence to Cassán Fabricio.

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Communicated by Erko Stackebrandt.

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Romina, M., Gastón, L., Belén, R. et al. Evaluation of growth and motility in non-photosynthetic Azospirillum brasilense exposed to red, blue, and white light. Arch Microbiol 202, 1193–1201 (2020). https://doi.org/10.1007/s00203-020-01829-8

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