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Specific hopanoid classes differentially affect free-living and symbiotic states of Bradyrhizobium diazoefficiens

Kulkarni, Gargi and Busset, Nicolas and Molinaro, Antonio and Gargani, Daniel and Chaintreuil, Clemence and Silipo, Alba and Giraud, Eric and Newman, Dianne K. (2015) Specific hopanoid classes differentially affect free-living and symbiotic states of Bradyrhizobium diazoefficiens. mBio, 6 (5). e01251-15. ISSN 2150-7511. PMCID PMC4620461.

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A better understanding of how bacteria resist stresses encountered during the progression of plant-microbe symbioses will advance our ability to stimulate plant growth. Here, we show that the symbiotic system comprising the nitrogen-fixing bacterium Bradyrhizobium diazoefficiens and the legume Aeschynomene afraspera requires hopanoid production for optimal fitness. While methylated (2Me) hopanoids contribute to growth under plant-cell-like microaerobic and acidic conditions in the free-living state, they are dispensable during symbiosis. In contrast, synthesis of extended (C35) hopanoids is required for growth microaerobically and under various stress conditions (high temperature, low pH, high osmolarity, bile salts, oxidative stress, and antimicrobial peptides) in the free-living state and also during symbiosis. These defects might be due to a less rigid membrane resulting from the absence of free or lipidA-bound C35 hopanoids or the accumulation of the C30 hopanoid diploptene. Our results also show that C35 hopanoids are necessary for symbiosis only with the host Aeschynomene afraspera but not with soybean. This difference is likely related to the presence of cysteine-rich antimicrobial peptides in Aeschynomene nodules that induce drastic modification in bacterial morphology and physiology. The study of hopanoid mutants in plant symbionts thus provides an opportunity to gain insight into host-microbe interactions during later stages of symbiotic progression, as well as the microenvironmental conditions for which hopanoids provide a fitness advantage.

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Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2015 Kulkarni et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Received 27 July 2015 Accepted 17 September 2015 Published 20 October 2015. This work was supported by awards from NASA (NNX12AD93G), the National Science Foundation (1224158), and the Howard Hughes Medical Institute (HHMI) to D.K.N.; the Agence Nationale de la Recherche, grant “BugsInACell” no. ANR-13-BSV7-0013, to E.G.; and the Italian Ministry of Education, Universities and Research (PRIN) and Mizutani Foundation for Glycoscience 2014 to A.M. and A.S. D.K.N. is an HHMI Investigator. The EM facility where the cryo-TEM micrographs were collected is supported by the Agouron and Beckman foundations. We thank Raphael Ledermann and Hans-Martin Fischer for providing strains and protocols and for performing confirmatory soybean symbiosis assays; Alasdair McDowell in Grant J. Jensen’s lab for collecting cryo-TEM micrographs at the EM facility; and Luisa Sturiale and Domenico Garozzo for recording the MS spectra. We are grateful to Newman lab members for constructive comments on the manuscript. G.K. and N.B. contributed equally to this article.
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Agence Nationale de la Recherche (ANR)ANR-13-BSV7-0013
Ministero dell'Istruzione, dell'Università e della Ricerca (MIUR)UNSPECIFIED
Mizutani Foundation for Glycoscience 2014UNSPECIFIED
Agouron InstituteUNSPECIFIED
Arnold and Mabel Beckman FoundationUNSPECIFIED
Issue or Number:5
PubMed Central ID:PMC4620461
Record Number:CaltechAUTHORS:20151008-142740942
Persistent URL:
Official Citation:Kulkarni G, Busset N, Molinaro A, Gargani D, Chaintreuil C, Silipo A, Giraud E, Newman DK. 2015. Specific hopanoid classes differentially affect free-living and symbiotic states of Bradyrhizobium diazoefficiens. mBio 6(5):e01251-15. doi:10.1128/mBio.01251-15.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:60919
Deposited By: Donna Wrublewski
Deposited On:08 Oct 2015 23:32
Last Modified:03 Oct 2019 09:02

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