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Enhancement of thiamine release during synthetic mutualism between Chlorella sorokiniana and Azospirillum brasilense growing under stress conditions

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Abstract

Thiamine release during synthetic mutualism between Chlorella sorokiniana co-immobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense was measured under stress conditions of pH, light intensity, and nitrogen starvation in short-term experiments. Thiamine release in the co-immobilized treatment was significantly higher at acidic pH compared to thiamine released by either microorganism alone. Under slightly alkaline pH, C. sorokiniana released the highest amount of thiamine. At stressful pH 6, the co-immobilized treatment released a higher quantity of thiamine than the sum of thiamine released by either microorganisms when immobilized separately. Release of thiamine by C. sorokiniana alone or co-immobilized was light intensity dependent; with higher the light intensity, more thiamine was released. Extreme light intensity negatively affected growth of the microalgae and release of thiamine. Nitrogen starvation during the first 24 h of culturing negatively affected release of thiamine by both microorganisms, where C. sorokiniana was more severely affected. Partial or continuous nitrogen starvation had similar negative effects on C. sorokiniana, but co-immobilization improved thiamine release. These results indicate that thiamine is released during synthetic mutualism between C. sorokiniana and A. brasilense, and this happens specifically during the alleviation of pH stress in the microalgae.

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Acknowledgments

At CIBNOR, we thank Manuel Moreno, Francisco Hernandez, and Juan-Pablo Hernandez for technical support and Ira Fogel for English and editorial suggestions. At Auburn University, we thank John Mcinroy for final English editing. Alejandro Palacios of the Autonomous University of Baja California Sur, La Paz, Mexico provided advice in statistical analysis. This study was supported by Consejo Nacional de Ciencia y Tecnologia of Mexico (CONACYT-Basic Science-2009, contract 164548) and time for writing by The Bashan Foundation, USA. O.A.P. was a recipient of a graduate fellowship (CONACYT 226169) and small periodic grants from the Bashan Foundation. This is contribution 2015-004 from the Bashan Institute of Science, USA.

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Authors and Affiliations

  1. Environmental Microbiology Group, The Northwestern Center for Biological Research (CIBNOR), Calle IPN 195, La Paz, B.C.S., 23096, Mexico

    Oskar A. Palacios, Yoav Bashan & Luz E. de-Bashan

  2. The Bashan Institute of Science, 1730 Post Oak Court, Auburn, AL, 36830, USA

    Yoav Bashan & Luz E. de-Bashan

  3. Department of Entomology and Plant Pathology, Auburn University, 209 Life Sciences Building, Auburn, AL, 36849, USA

    Yoav Bashan & Luz E. de-Bashan

  4. German Research Center for Environmental Health, Department for Environmental Sciences, Research Unit Microbe–Plant Interactions, Helmholtz Zentrum München, Ingolstaedter Landstrasse 1, 85764, Neuherberg, Germany

    Michael Schmid & Anton Hartmann

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  1. Oskar A. Palacios
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  2. Yoav Bashan
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  5. Luz E. de-Bashan
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Correspondence to Luz E. de-Bashan.

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This study is dedicated to the memory of the German/Spanish mycorrhizae researcher Dr. Horst Vierheilig (1964–2011) of CSIC, Spain

The term “release” stands for “extrusion”, “excretion”, and “produce”. A specific term is used when the exact mechanism is known.

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Fig. S1

Comparison of thiamine release by Chlorella sorokiniana and Azospirillum brasilense at different pH of the medium when immobilized separately or immobilized together in alginate beads (a, b, c) and growth of these microorganisms in these cultures (d, e, f). Values along curves denoted by different capital letters differ significantly using one-way ANOVA and LSD post hoc analysis at P <0.05. Points at each time interval denoted by different lower case letters differ significantly at P <0.05 by the same statistical analyses. Bars represent SE. (PDF 262 kb)

Fig. S2

Comparison of thiamine content in exudates under different light intensities released by Chlorella sorokiniana (a), Azospirillum brasilense (b) immobilized alone and co-immobilized (c) and comparison of growth of these microorganisms in these cultures (d, e, f). Values along curves denoted by different capital letters differ significantly using one-way ANOVA and LSD post hoc analysis at P <0.05. Points at each time interval denoted by different lower case letters differ significantly at P <0.05 by the same statistical analyses. Bars represent SE. (PDF 270 kb)

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Palacios, O.A., Bashan, Y., Schmid, M. et al. Enhancement of thiamine release during synthetic mutualism between Chlorella sorokiniana and Azospirillum brasilense growing under stress conditions. J Appl Phycol 28, 1521–1531 (2016). https://doi.org/10.1007/s10811-015-0697-z

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