Abstract
ABSTRACTPlant 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 microbiota assembly and suggest that the observed interaction between tobacco and Arthrobacter may be a consequence of an ecological fitting process.
Highlights
IMPORTANCE Host secondary metabolites have a crucial effect on the taxonomic composition of its associated microbiota
Analysis of taxonomic profiles across samples by fitting normalized read counts to a generalized linear model (GLM) with a negative binomial distribution revealed that the bacterial members belonging to the order Actinomycetales were most significantly enriched in the endosphere compared to the rhizosphere and rhizoplane fractions (Fig. 1B)
We found that the Micrococcaceae family was the only family enriched both in the tobacco endosphere compared to the rhizoplane and commonly by santhopine and nicotine treatments (Fig. 2A and Data Set S1) in a dose-dependent manner (Fig. S1C and D)
Summary
IMPORTANCE Host secondary metabolites have a crucial effect on the taxonomic composition of its associated microbiota. 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 Plant roots secrete their photosynthates to the rhizosphere, a fraction of soil surrounding the root [1], creating a nutrient-rich environment with a distinctive metabolic profile compared to the bulk soil [2, 3]. Plant specialized metabolites (PSMs), known as plant secondary metabolites, play an important role in the interaction between the host and its root microbiota, affecting its taxonomic composition [9, 10]. Nicotine is catabolized by several bacterial species [33, 34], implying the possible involvement of both santhopine and nicotine in the interaction between tobacco and its root-associated microbiota
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