Universität zu Köln

Shimasaki, Tomohisa, Masuda, Sachiko, Garrido-Oter, Ruben, Kawasaki, Takashi, Aoki, Yuichi, Shibata, Arisa, Suda, Wataru, Shirasu, Ken ORCID: 0000-0002-0349-3870, Yazaki, Kazufumi, Nakano, Ryohei Thomas ORCID: 0000-0001-5973-2300 and Sugiyama, Akifumi (2021). Tobacco Root Endophytic Arthrobacter Harbors Genomic Features Enabling the Catabolism of Host-Specific Plant Specialized Metabolites. mBio, 12 (3). WASHINGTON: AMER SOC MICROBIOLOGY. ISSN 2150-7511

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Abstract

Plant roots constitute the primary interface between plants and soilborne microorganisms and harbor microbial communities called the root microbiota. Recent studies have demonstrated a significant contribution of plant specialized metabolites (PSMs) to the assembly of root microbiota. However, the mechanistic and evolutionary details underlying the PSM-mediated microbiota assembly and its contribution to host specificity remain elusive. Here, we show that the bacterial genus Arthrobacter is predominant specifically in the tobacco endosphere and that its enrichment in the tobacco endosphere is partially mediated by a combination of two unrelated classes of tobacco-specific PSMs, santhopine and nicotine. We isolated and sequenced Arthrobacter strains from tobacco roots as well as soils treated with these PSMs and identified genomic features, including but not limited to genes for santhopine and nicotine catabolism, that are associated with the ability to colonize tobacco roots. Phylogenomic and comparative analyses suggest that these genes were gained in multiple independent acquisition events, each of which was possibly triggered by adaptation to particular soil environments. Taken together, our findings illustrate a cooperative role of a combination of PSMs in mediating plant species-specific root bacterial micro biota assembly and suggest that the observed interaction between tobacco and Arthrobacter may be a consequence of an ecological fitting process. IMPORTANCE Host secondary metabolites have a crucial effect on the taxonomic composition of its associated microbiota. It is estimated that a single plant species produces hundreds of secondary metabolites; however, whether different classes of metabolites have distinctive or common roles in the microbiota assembly remains unclear. Here, we show that two unrelated classes of secondary metabolites in tobacco play a cooperative role in the formation of tobacco-specific compositions of the root bacterial microbiota, which has been established as a consequence of independent evolutionary events in plants and bacteria triggered by different ecological effects. Our findings illustrate mechanistic and evolutionary aspects of the microbiota assembly that are mediated by an arsenal of plant secondary metabolites.

Item Type:	Journal Article
Creators:	Creators Email ORCID ORCID Put Code Shimasaki, Tomohisa UNSPECIFIED UNSPECIFIED UNSPECIFIED Masuda, Sachiko UNSPECIFIED UNSPECIFIED UNSPECIFIED Garrido-Oter, Ruben UNSPECIFIED UNSPECIFIED UNSPECIFIED Kawasaki, Takashi UNSPECIFIED UNSPECIFIED UNSPECIFIED Aoki, Yuichi UNSPECIFIED UNSPECIFIED UNSPECIFIED Shibata, Arisa UNSPECIFIED UNSPECIFIED UNSPECIFIED Suda, Wataru UNSPECIFIED UNSPECIFIED UNSPECIFIED Shirasu, Ken UNSPECIFIED orcid.org/0000-0002-0349-3870 UNSPECIFIED Yazaki, Kazufumi UNSPECIFIED UNSPECIFIED UNSPECIFIED Nakano, Ryohei Thomas UNSPECIFIED orcid.org/0000-0001-5973-2300 UNSPECIFIED Sugiyama, Akifumi UNSPECIFIED UNSPECIFIED UNSPECIFIED
URN:	urn:nbn:de:hbz:38-586964
DOI:	10.1128/mBio.00846-21
Journal or Publication Title:	mBio
Volume:	12
Number:	3
Date:	2021
Publisher:	AMER SOC MICROBIOLOGY
Place of Publication:	WASHINGTON
ISSN:	2150-7511
Language:	English
Faculty:	Unspecified
Divisions:	Unspecified
Subjects:	no entry
Uncontrolled Keywords:	Keywords Language AMINO-ACIDS; T-DNA; BACTERIAL; NICOTINE; MICROBIOTA; EXPRESSION; NUTRITION; OXIDASE; PROTEIN; GENES Multiple languages Microbiology Multiple languages
URI:	http://kups.ub.uni-koeln.de/id/eprint/58696