Widespread horizontal gene transfer between plants and their microbiota

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Plants host a large array of commensal bacteria that interact with the host. The growth of both bacteria and plants is often dependent on nutrients derived from the cognate partners, and the bacteria fine-tune host immunity against pathogens. This ancient interaction is common in all studied land plants and is critical for proper plant health and development. We hypothesized that the spatial vicinity and the long-term relationships between plants and their microbiota may promote or even depend on cross-kingdom horizontal gene transfer (HGT), a phenomenon that is relatively rare in nature. To test this hypothesis we analyzed the Arabidopsis thaliana genome and its extensively sequenced microbiome to detect events of horizontal transfer of full length genes that are absent from non-plant associated bacteria. Interestingly, we detected 180 unique genes that were horizontally transferred between plants and their microbiota. Genes transferred from plants to their microbiota are enriched in secreted proteins that metabolize carbohydrates, whereas microbes transferred to plants genes that are enriched in redox homeostasis functions. To validate our approach, we tested if a bacterial gene is functionally similar to its Arabidopsis homologue in planta . The Arabidopsis DET2 gene is essential for biosynthesis of the brassinosteroid phytohormones and loss-of-function of the gene leads to dwarfism. We found that expression of the DET2 homologue from Leifsonia bacteria of the Actinobacteria phylum in the Arabidopsis det2 background complements the mutant, and leads to normal plant growth. Together, these data suggest that cross-kingdom horizontal gene transfer events shape the interactions between plants and their microbiome.

Significance statement

What are the genes that shape host-microbe interactions and what are their origins are fundamental questions in molecular ecology and evolution. We explored the evolutionary mechanisms that formed Arabidopsis-microbiota interactions, as a model for host-microbe interactions. We found prevalent horizontal gene transfer, affecting 180 genes, that occurred between plants and their commensal microbiota. We propose that these genes participate in molecular mimicry between the host and its microbiome. Bacteria acquired from plants genes that primarily encode for secreted proteins that metabolize carbohydrates, thereby enabling bacteria to grow on plant-derived sugars. Additionally, we demonstrate how a bacterial gene that mimics a plant hormone biosynthesis gene can replace the plant gene function. Our results suggest that horizontal gene transfer between hosts and their microbiota is a significant and active evolutionary mechanism that contributed new traits to plants and their commensal microbiota.

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  1. These resultsalso support our current results that nearly all transfers into Arabidopsis are ancient andare shared by monocots and dicots. We could not detect a bacterial gene that wastransferred directly to Brassicaceae and is absent from other dicots.

    Very helpful statement! I think this also says something interesting about your methods. For "ancient" HGT events, it doesn't matter that much what plant genome you look at to identify them

  2. Interestingly, this level of sequence similarity is shared between theArabidopsis DET2 and its homologues from rice and barley. Importantly, the proteinsfrom other eukaryotic plant pathogens such as Phytophthora and Pythium share weakeridentity (maximum 41% identity) to the Arabidopsis protein than theLeifsonia-Arabidopsis DET2 similarity.

    This is a little hard to interpret as written. Does this suggest that Arabidopsis DET2 was the acceptor of Leifsonia DET2, or that the transfer may have occurred at the LCA between Arabidopsis and rice and barley?

  3. Tosummarize this analysis, in most cases the taxonomy of the bacterial donor or acceptoris unknown, and Actinobacteria and Proteobacteria relatively rarely donate or acceptgenes from plants.

    It could be interesting to complement this type of analysis by looking at GC content or tetramernucleotide frequency in this gene across genomes, and how that compares to host genome background. How similar are these genes to the rest of the genes in a given bacteria's genome?

  4. Using the current taxonomicinformation we cannot tell if this HGT pattern is the result of gene transfer to onemicrobial phylum followed by an additional transfer to another microbial phylum, orindependent gene transfer event to multiple phyla.

    Is there any information that does exist that would allow you to have a better understanding of this? For example, I'm guessing a lot of the microbes you looked at have other isolate genomes sequences in public databases; could you potentially do a pangenome analysis to help understand the trends you identified? (not suggesting you do this for this paper! But I think this is interesting to brainstorm around and might warrant an additional sentence of potential future methods someone could use to answer this type of question)

  5. We analyzed the number of introns foundin Arabidopsis genes transferred from PA bacteria assuming that they would containless introns than the average plant gene. However, we found no statistical differencebetween the number of introns of horizontally transferred genes and all otherArabidopsis genes (Supplementary Figure 16).

    Very cool/clever!

  6. A.

    I found myself a little confused by the box in the second row on the left hand side. Is this an outline of results as well? Or did you determine which 582 plant associated proteins to screen? or is this 582 bacteria?

  7. Bacteria acquired from plants genes that primarily encode for secreted proteins thatmetabolize carbohydrates, thereby enabling bacteria to grow on plant-derived sugars.

    This sentence was a little hard to understand, I found myself reading it a few times to make sure I grasped the meaning...but it's an important point! I wonder if it can be rephrased? maybe removing "from" at the beginning of the sentence would help?

  8. However, we did not identifybacterial-Arabidopsis homologous protein pairs with amino acid identity above 76%,rejecting the possibility of hypothetical DNA contamination which would lead to highlysimilar protein sequences

    This is a really helpful statement and something I was really curious about -- contamination is always a super hard thing to separate from HGT. I wonder if it would be easy to filter this analysis to only long read genomes, and to look at the identity of nearby proteins to the candidate HGTs. Barring misassemblies/chimeric contigs, it might be easier to trace the HGT events in longer reads. Probably not necessary here, just brainstorming about alternate signals that could really solidify that these candidates are HGT and not contam!