LEY 25113 PDF

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Plants intimately associate with diverse bacteria. Plant-associated PA bacteria have ostensibly evolved genes enabling adaptation to the plant environment. However, the identities of such genes are mostly unknown and their functions are poorly characterized.

Genomic features of bacterial adaptation to plants

We sequenced genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared bacterial genomes to identify thousands of PA gene clusters. Genomes of PA bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant associated genomes. We experimentally validated candidates from two sets of PA genes, one involved in plant colonization, the other serving in microbe-microbe competition between PA bacteria.

We also identified 64 PA protein domains that potentially mimic plant domains; some are shared with PA fungi and oomycetes.

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This work expands the genome-based understanding of plant-microbe interactions and provides leads for efficient and sustainable agriculture through microbiome engineering. The microbiota of plants and animals have co-evolved with their hosts for millions of years 1 — 3. Due to photosynthesis, plants serve as a rich source of carbon for diverse bacterial communities. These include mutualists and commensals, as well as pathogens. Phytopathogens and plant growth-promoting bacteria significantly affect plant growth, health, and productivity 4 — 7.

Except for intensively studied relationships such as root nodulation in legumes 8T-DNA transfer by Agrobacterium ,eyand type III secretion-mediated pathogenesis 10the understanding of molecular mechanisms governing plant-microbe interactions is quite limited.

It is therefore important to identify and characterize the bacterial genes and functions that help microbes thrive in the plant environment. Such knowledge should improve our ability to combat plant diseases and harness beneficial bacterial functions for agriculture, directly impacting global food security, bioenergy, and carbon sequestration. Cultivation-independent methods based on profiling of marker genes or shotgun metagenome sequencing have considerably improved our understanding of microbial ecology in the plant environment 11 — In parallel, the reduction of sequencing costs has enabled the genome sequencing of plant-associated PA bacterial isolates at a large scale Importantly, isolates enable functional validation of in silico predictions.

Isolate genomes also provide genomic and evolutionary context for individual genes and the ability to access genomes of rare organisms that might be missed by metagenomics due to limited sequencing depth.

While metagenome sequencing has the advantage of capturing the DNA of uncultivated organisms, multiple 16S rRNA gene surveys have reproducibly 2113 that the most common plant-associated bacteria are mainly derived from four phyla 1317 Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes that are amenable to cultivation. Thus, bacterial cultivation is not a major limitation when sampling the abundant members of the plant microbiome Our objective was to characterize the genes that contribute to bacterial adaptation to lley plant-associated genes and those genes that specifically aid in bacterial root colonization root-associated genes.

We sequenced the genomes of new bacterial isolates and single bacterial cells from the roots of Brassicaceae, maize, and poplar trees. We combined the newly sequenced with existing genomes into a dataset of high quality, non-redundant genomes.

We then developed a computational approach to ely plant-associated PA genes and root-associated RA genes based on comparison of phylogenetically-related genomes with knowledge of the origin of isolation. We experimentally validated two sets of PA genes, including a novel gene family 251133 functions in plant-associated microbe-microbe competition. In addition, we characterized many PA genes that are shared between bacteria of different phyla and even between bacteria and PA eukaryotes.

This study represents a comprehensive and unbiased effort to identify and characterize candidate genes required at the bacterial-plant interface. The bacteria were specifically isolated from either the root interior endophytic compartmentthe root surface rhizoplaneor the soil attached to the root rhizosphere of plants. In addition, we isolated and sequenced single bacterial cells from surface-sterilized roots of A. All genomes were assembled, annotated and deposited in public databases and in a dedicated website see URLs, Supplementary Table 3Methods.


Novel and previously sequenced and genomes used in this analysis. Taxon color denotes phylum: PA — plant-associated bacteria, NPA — non-plant associated bacteria, soil — soil associated bacteria, RA- root-associated bacteria. NA — not available an artificial taxon. In addition to the newly sequenced genomes noted above, we mined public databases to collect bacterial genomes lye to the four most abundant phyla of PA bacteria 13 Methods.

We manually classified each genome as PA, non-plant associated Leeyor soil-derived based on its unambiguous isolation niche Methods, Supplementary Tables The PA genomes included organisms isolated from plants or rhizospheres. Genomes from bacteria isolated from soil were considered as a separate group, as it is unknown whether these strains can actively associate with plants.

Finally, the remaining genomes 25113 labeled as non-plant associated NPA genomes; these were isolated from diverse environments, including humans, animals, air, sediments, and aquatic environments. We performed a stringent quality control process to remove low quality or redundant genomes Methods.

This led to a final dataset of high quality and non-redundant genomes, 25113 PA genomes, of which are also Oey. These genomes were grouped into nine monophyletic taxa to allow comparative genomics among phylogenetically-related genomes Figure 1aSupplementary TablesMethods, URLs. Maximum likelihood phylogenetic tree of high quality and non-redundant bacterial genomes based on the concatenated alignment of 31 single copy genes. Outer ring denotes the taxonomic group, central ring denotes the isolation source, and inner ring denotes the RA genomes within PA genomes.

Taxon names are color-coded based on phylum: For both panels, the heat map indicates the level of enrichment or depletion based on a PhyloGLM test.

Hot colored cells indicate significantly more genes in PA and RA genomes in the upper and lower panels, respectively. Histograms on the upper and right margins represent the total number of genes compared in each column and row, respectively. Carbohydrates — Carbohydrate metabolism and transport gene category. Note that cells with high absolute estimate values dark colors are based on categories of few genes and are therefore more likely to be less accurate. To determine whether our genome collection from cultured isolates is representative of plant-associated bacterial communities, we analyzed cultivation-independent 16S rDNA surveys and metagenomes from the plant environment of Arabidopsis 1112barley 18wheat, and cucumber 14 Methods.

We compared the genomes of bacteria isolated from plant environments with bacteria of shared ancestry yet isolated from non-plant environments. The two groups should differ in the set of accessory genes that evolved as part of their adaptation to a specific niche.

The trend was observed in of the nine analyzed taxa depending on the testrepresenting all four phyla. Next, we examined whether certain gene categories are enriched or depleted in PA genomes compared to their NPA counterparts, using 26 broad functional gene categories Supplementary Table 6. Two gene categories demonstrated similar phylogeny-independent trends suggestive of an environment-dependent selection process. This was the most expanded category in Alphaproteobacteria, Bacteroidetes, Xanthomonadaceae, and Pseudomonas Supplementary Figure 3upper panel.

In contrast, mobile genetic elements phages and transposons were underrepresented in four PA taxa Figures 1b and Supplementary Figure 3upper panels. Interestingly, PA genomes exhibited increased genome sizes despite a reduction in the mobile elements that often serve as vehicles for horizontal gene transfer and genome expansion.

Comparison of RA bacteria to soil bacteria revealed less drastic changes than those seen between PA and NPA groups, as expected for lye that live in more similar habitats Figures 1b and Supplementary Figure 3lower panels.

In order to capture in our analysis genes that do not have existing functional annotations, we also used Orthofinder 24 following benchmarking; Supplementary Figure 5 to cluster all protein sequences within each taxon into homology-based orthogroups. Significant gene clusters found using the different methods had varying lye of overlap Supplementary Figure We retrieved 38 publicly available PA, NPA, RA and soil shotgun metagenomes, including some from PA environments that were not used for isolation of the bacteria analyzed here 142829 Supplementary Table 16a.


We mapped reads from these culture-independent metagenomes to PA genes from all statistical approaches Methods, Supplementary Figures RA, soil-associated and NPA genes, on the other hand, were not necessarily more abundant in their expected environments Supplementary Table 16b. Full results and explanation for normalization are presented in Supplementary Figure Rice root colonization experiment using wild type Paraburkholderia kururiensis M or knockout mutants for two predicted PA genes.

Two mutants exhibited reduced colonization in comparison to wild type: Examples of known functional PA operons captured by different statistical approaches.

The PA genes are underlined. Chemotaxis proteins in bacteria from different taxa. Type III secretion leh. Type VI secretion system, including the imp genes imp aired lye nodulationi.

Flagellum biosynthesis in Alphaproteobacteria. Below each gene appears the gene symbol le the protein name where such information was available.

In addition, we selected eight genes that were predicted as PA by multiple approaches Supplementary Table 17a for experimental validation using 25131 in planta bacterial fitness assay Methods. We grew the plants for 11 days, collected and quantified the bacteria that were tightly attached to the roots Methods, Supplementary Table 17b.

Genomic features of bacterial adaptation to plants

These two genes encode an outer membrane efflux transporter from the nodT family and a Tir chaperone protein CesT. It is plausible that the other six genes assayed function in facets of plant association not captured in this experimental context. Functions for which co-expression and cooperation between different proteins are needed are often encoded by gene operons in bacteria. We therefore tested whether our methods correctly predict known PA operons.

Nod and Nif proteins are integral for biological nitrogen cycling, mediating root nodulation 31 and nitrogen fixation 32respectively. We also identified the biosynthetic gene cluster for the precursor leg the plant hormone gibberellin 3334 Figure 2e. Other known PA operons identified are related to chemotaxis of diverse bacteria 35secretion systems such as T3SS 36 and T6SS 37and flagellum biosyntheis 38 — 40 Figure 2f-i.

In summary, we identified thousands of PA and RA gene clusters by five different statistical approaches Supplementary Table 18 and validated these by computational and experimental approaches, broadening our understanding of the genetic basis of plant-microbe interactions and providing a valuable resource to drive further experimentation.

PA and RA proteins and protein domains conserved across evolutionarily diverse taxa are potentially pivotal to the interaction of bacteria with plants. 251133 identified Pfam domains that are significant PA domains in at least three taxa based on multiple tests Supplementary Table 19a.

Two of these domains, a DNA binding pfam and a ligand binding pfam domain, are characteristic of the LacI transcription factor TF family. These TFs regulate gene expression in response to different sugars 41 and their copy number is expanded in the genomes of PA and RA bacteria of eight of the nine taxa analyzed Figure 3a. Examination of the genomic neighbors of lacI family genes revealed a strong enrichment for genes involved in carbohydrate metabolism and transport in all of these taxa, consistent with their expected regulation by a LacI family member 41 Supplementary Figure These data suggest that accumulation of a large repertoire of LacI-family controlled regulons is a common strategy across bacterial lineages as they adapt to the plant environment.

Taxon names are color coded by phyla as in Figure 1. Transcription factors having LacI Pfam and periplasmic binding protein domains Pfam These proteins are often annotated as COG Aldo-keto reductase domain Pfam Proteins with this domain are often annotated as COG A two-sided t -test was used for the presence of the genes in a-b between the genomes sharing the same label and was used to verify the enrichment reported by the various tests.