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Patterns of transmission and horizontal gene transfer in the Dioscorea sansibarensis leaf symbiosis revealed by whole-genome sequencing.

Authors
  • Danneels, Bram1
  • Viruel, Juan2
  • Mcgrath, Krista3
  • Janssens, Steven B4
  • Wales, Nathan5
  • Wilkin, Paul2
  • Carlier, Aurélien6
  • 1 Laboratory of Microbiology, Ghent University, 9000 Ghent, Belgium. , (Belgium)
  • 2 Royal Botanical Gardens, Kew, Richmond, Surrey TW9 3AE, UK.
  • 3 Department of Prehistory and Institute of Environmental Science and Technology (ICTA), Autonomous University of Barcelona, 08193 Bellaterra, Spain; Department of Archaeology, University of York, Heslington, York YO10 5DD, UK. , (Spain)
  • 4 Meise Botanic Garden, 1860 Meise, Belgium; Department of Biology, KU Leuven, 3000 Leuven, Belgium. , (Belgium)
  • 5 Department of Archaeology, University of York, Heslington, York YO10 5DD, UK.
  • 6 Laboratory of Microbiology, Ghent University, 9000 Ghent, Belgium; LIPME, Université de Toulouse, INRAE, CNRS, 31320 Castanet-Tolosan, France. Electronic address: [email protected] , (Belgium)
Type
Published Article
Journal
Current biology : CB
Publication Date
Jun 21, 2021
Volume
31
Issue
12
Identifiers
DOI: 10.1016/j.cub.2021.03.049
PMID: 33852872
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

Leaves of the wild yam species Dioscorea sansibarensis display prominent forerunner or "drip" tips filled with extracellular bacteria of the species Orrella dioscoreae.1 This species of yam is native to Madagascar and tropical Africa and reproduces mainly asexually through aerial bulbils and underground tubers, which also contain a small population of O. dioscoreae.2,3 Despite apparent vertical transmission, the genome of O. dioscoreae does not show any of the hallmarks of genome erosion often found in hereditary symbionts (e.g., small genome size and accumulation of pseudogenes).4-6 We investigated here the range and distribution of leaf symbiosis between D. sansibarensis and O. dioscoreae using preserved leaf samples from herbarium collections that were originally collected from various locations in Africa. We recovered DNA from the extracellular symbiont in all samples, showing that the symbiosis is widespread throughout continental Africa and Madagascar. Despite the degraded nature of this DNA, we constructed 17 symbiont genomes using de novo methods without relying on a reference. Phylogenetic and genomic analyses revealed that horizontal transmission of symbionts and horizontal gene transfer have shaped the evolution of the symbiont. These mechanisms could help explain lack of signs of reductive genome evolution despite an obligate host-associated lifestyle. Furthermore, phylogenetic analysis of D. sansibarensis based on plastid genomes revealed a strong geographical clustering of samples and provided evidence that the symbiosis originated at least 13 mya, earlier than previously estimated.3. Copyright © 2021 Elsevier Inc. All rights reserved.

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