Evolutionary stability of antibiotic protection in a defensive symbiosis
Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved January 18, 2018 (received for review November 15, 2017)
Significance
Insights from natural applications of antibiotics are important to gain a deeper understanding of the evolutionary processes that underlie the maintenance of an antibiotic defense and prevent the rise and spread of antibiotic resistance. Using 25 species and subspecies of beewolf digger wasps that engage in a defensive symbiosis with Streptomyces bacteria, we tracked evolutionary changes in the antibiotic cocktail that protects the wasps’ larval offspring against mold fungi. Our results yield insights into the mechanistic basis as well as the ecological and evolutionary implications of producing a complex cocktail of antimicrobial compounds in a symbiotic setting.
Abstract
The increasing resistance of human pathogens severely limits the efficacy of antibiotics in medicine, yet many animals, including solitary beewolf wasps, successfully engage in defensive alliances with antibiotic-producing bacteria for millions of years. Here, we report on the in situ production of 49 derivatives belonging to three antibiotic compound classes (45 piericidin derivatives, 3 streptochlorin derivatives, and nigericin) by the symbionts of 25 beewolf host species and subspecies, spanning 68 million years of evolution. Despite a high degree of qualitative stability in the antibiotic mixture, we found consistent quantitative differences between species and across geographic localities, presumably reflecting adaptations to combat local pathogen communities. Antimicrobial bioassays with the three main components and in silico predictions based on the structure and specificity in polyketide synthase domains of the piericidin biosynthesis gene cluster yield insights into the mechanistic basis and ecoevolutionary implications of producing a complex mixture of antimicrobial compounds in a natural setting.
Data Availability
Data deposition: The data reported in this paper have been deposited in GenBank, https://www.ncbi.nlm.nih.gov/genbank (accession nos. KX098584, KU759552–KU759556, and KU759557–KU759562). The MS data reported in this paper have been deposited in the Dryad Digital Repository (doi:https://doi.org/10.5061/dryad.6907h).
Acknowledgments
We thank Christine Michel, Fred and Sarah Gess, Sabrina Koehler, Gudrun Herzner, Dirk Koedam, and Erol Yildirim for help with field work or generous gifts of specimens. We also thank Riya Christina Menezes for help with the verification of nigericin and Jörn Piel for his constructive comments on the manuscript. Permits were issued by the nature conservation boards of KwaZulu Natal (Permit 4362/2004), Eastern Cape Province (WRO44/04WR, WRO9/04WR,WRO74/06WR, WRO75/06WR, CRO135/11CR, CRO136/11CR, CRO179/10CR, and CRO180/10CR), and Western Cape Province (001-202-00026, 001-506-00001, AAA004-00053-0035, AAA004-00089-0011, AAA004-00683-0035, and 0046-AAA004-00008) of South Africa and the Brazilian Ministry of the Environment (MMA/SISBIO/22861-1). We acknowledge financial support from the Max Planck Society and German Science Foundation Grant DFG KA2846/2-1 (to M. Kaltenpoth).
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© 2018. Published under the PNAS license.
Data Availability
Data deposition: The data reported in this paper have been deposited in GenBank, https://www.ncbi.nlm.nih.gov/genbank (accession nos. KX098584, KU759552–KU759556, and KU759557–KU759562). The MS data reported in this paper have been deposited in the Dryad Digital Repository (doi:https://doi.org/10.5061/dryad.6907h).
Submission history
Published online: February 14, 2018
Published in issue: February 27, 2018
Keywords
Acknowledgments
We thank Christine Michel, Fred and Sarah Gess, Sabrina Koehler, Gudrun Herzner, Dirk Koedam, and Erol Yildirim for help with field work or generous gifts of specimens. We also thank Riya Christina Menezes for help with the verification of nigericin and Jörn Piel for his constructive comments on the manuscript. Permits were issued by the nature conservation boards of KwaZulu Natal (Permit 4362/2004), Eastern Cape Province (WRO44/04WR, WRO9/04WR,WRO74/06WR, WRO75/06WR, CRO135/11CR, CRO136/11CR, CRO179/10CR, and CRO180/10CR), and Western Cape Province (001-202-00026, 001-506-00001, AAA004-00053-0035, AAA004-00089-0011, AAA004-00683-0035, and 0046-AAA004-00008) of South Africa and the Brazilian Ministry of the Environment (MMA/SISBIO/22861-1). We acknowledge financial support from the Max Planck Society and German Science Foundation Grant DFG KA2846/2-1 (to M. Kaltenpoth).
Notes
This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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