Automated reconstruction of all gene histories in large bacterial pangenome datasets and search for co-evolved gene modules with Pantagruel

Lassalle, Florent; Veber, Philippe; Jauneikaite, Elita; Didelot, Xavier

doi:10.1101/586495

Cited by 15 publications

(18 citation statements)

References 29 publications

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“…A custom set of 155 genomes was gathered covering 28 different Bradyrhizobium species, as well as selected genomes from the genera Nitrobacter and Rhodopseudomonas as outgroups. The genomes listed in Table S1 (available in the online version of this article) were downloaded from the National Center for Biotechnology Information (NCBI) RefSeq or GenBank databases and used as input for the bioinformatic pipeline Pantagruel [26] to build a phylogenomic database. In short, coding sequences (CDSs) and the corresponding protein sequences were extracted from the RefSeq or GenBank annotation and then clustered into homologous gene families using MMSeqs2 [27].…”

Section: Methodsmentioning

confidence: 99%

“…Bayesian scenario samples were used to compute co-evolution scores between gene families, using an approach adapted from Lassalle et al . [26] and detailed further in File S1. ML and Bayesian samples of scenarios, summaries of the inferred transfer events and of the co-evolution analysis are available as part of online Supporting Data at the Figshare data repository (http://dx.doi.org/10.6084/m9.figshare.12191103).…”

Section: Methodsmentioning

confidence: 99%

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Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

et al. 2020

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Bradyrhizobium are abundant soil bacteria and the major symbiont of legumes. The recent availability of Bradyrhizobium genome sequences provides a large source of information for analysis of symbiotic traits. In this study, we investigated the evolutionary dynamics of the nodulation genes (nod) and their relationship with the genes encoding type III secretion systems (T3SS) and their effectors among bradyrhizobia. Based on the comparative analysis of 146 Bradyrhizobium genome sequences, we identified six different types of T3SS gene clusters. The two predominant cluster types are designated RhcIa and RhcIb and both belong to the RhcI-T3SS family previously described in other rhizobia. They are found in 92/146 strains, most of them also containing nod genes. RhcIa and RhcIb gene clusters differ in the genes they carry: while the translocon-encoding gene nopX is systematically found in strains containing RhcIb, the nopE and nopH genes are specifically conserved in strains containing RhcIa, suggesting that these last two genes might functionally substitute nopX and play a role related to effector translocation. Phylogenetic analysis suggests that bradyrhizobia simultaneously gained nod and RhcI-T3SS gene clusters via horizontal transfer or subsequent vertical inheritance of a symbiotic island containing both. Sequence similarity searches for known Nop effector proteins in bradyrhizobial proteomes revealed the absence of a so-called core effectome, i.e. that no effector is conserved among all Bradyrhizobium strains. However, NopM and SUMO proteases were found to be the main effector families, being represented in the majority of the genus. This study indicates that bradyrhizobial T3SSs might play a more significant symbiotic role than previously thought and provides new candidates among T3SS structural proteins and effectors for future functional investigations.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

et al. 2020

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“…Further pangenome analyses were conducted using the Pantagruel pipeline under the default settings as described previously (Lassalle et al, 2019, Lassalle et al, 2020) and on the program webpage http://github.com/flass/pantagruel/. Because of computationally highly intensive tasks, the dataset analyzed was limited to the Allorhizobium genus and Rhizobium aggregatum complex (total of 28 strains).…”

Section: Methodsmentioning

confidence: 99%

Genomic analysis provides novel insights into diversification and taxonomy ofAllorhizobium vitis(i.e.Agrobacterium vitis)

Kuzmanović

Biondi

Overmann

et al. 2020

Preprint

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Allorhizobium vitis (formerly named Agrobacterium vitis or Agrobacterium biovar 3) is the primary causative agent of crown gall disease of grapevine worldwide. Whole-genome sequence comparisons and phylogenomic analysis of various All. vitis strains clearly indicated that All. vitis is not a single species, but represents a species complex composed of at least four genomic species. Thus, we amended the description of All. vitis which now refers to a restricted group of strains within the All. vitis complex (i.e. All. vitis sensu stricto) and proposed a description of a novel species All. ampelinum sp. nov. The type strain of All. vitis sensu stricto remains the existing type strain of All. vitis, K309T (= NCPPB 3554T =HAMBI 1817T = ATCC 49767T = CIP 105853T = ICMP 10752T = IFO 15140T = JCM 21033T = LMG 8750T = NBRC 15140T). The type strain of All. ampelinum sp. nov. is S4T (= DSM 112012T = ATCCBAA-846T). This genome-based classification was supported by differentiation of strains based on a MALDI-TOF MS analysis. We also identified gene clusters specific for All. vitis species complex, All. vitis sensu stricto and All. ampelinum, and attempted to predict their function and their role in ecological diversification of these clades, some of which were experimentally validated. Functions of All. vitis species complex-specific genes convergently indicate a role in adaptation to different stresses, including exposure to aromatic compounds. Similarly, All vitis sensu stricto-specific genes also confer the ability to degrade 4-hydroxyphenylacetate and a putative compound related to gentisic acid, while All. ampelinum-specific genes have putative functions related to polyamine metabolism and nickel assimilation. This suggests that these species have differentiated ecologies, each relying on specialized nutrient consumption or toxic compound degradation to adapt to their respective niche. Moreover, our genome-based analysis indicated that Allorhizobium and the “R. aggregatum complex” represent separate genera of the family Rhizobiaceae.

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“…Unless specified otherwise, the following bioinformatic analyses were conducted using the Pantagruel pipeline under the default settings as described previously [23] and on the program webpage http://github.com/flass/pantagruel/. This pipeline is designed for the analysis of bacterial pangenomes, including the inference of a species tree, gene trees, and the detection of horizontal gene transfers (HGT) through species tree/gene tree reconciliations [62].…”

Section: Methodsmentioning

confidence: 99%

Phylogenomic analysis reveals the basis of adaptation of Pseudorhizobium species to extreme environments

Lassalle

Smm²,

Zhao

et al. 2019

Preprint

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AbstractThe family Rhizobiaceae includes many genera of soil bacteria, often isolated for their association with plants. Herein, we investigate the genomic diversity of a group of Rhizobium species and unclassified strains isolated from atypical environments, including seawater, rock matrix or polluted soil. Based on whole-genome similarity and core genome phylogeny, we show that this group corresponds to the genus Pseudorhizobium. We thus reclassify Rhizobium halotolerans, R. marinum, R. flavum and R. endolithicum as P. halotolerans comb. nov., P. marinum comb. nov., P. flavum comb. nov. and R. endolithicum comb. nov., respectively, and show that P. pelagicum is a synonym of P. marinum. We also delineate a new chemolithoautotroph species, P. banfieldiae sp. nov., whose type strain is NT-26T (= DSM 106348T = CFBP 8663T). This genome-based classification was supported by a chemotaxonomic comparison, with gradual taxonomic resolution provided by fatty acid, protein and metabolic profiles. In addition, we used a phylogenetic approach to infer scenarios of duplication, horizontal transfer and loss for all genes in the Pseudorhizobium pangenome. We thus identify the key functions associated with the diversification of each species and higher clades, shedding light on the mechanisms of adaptation to their respective ecological niches. Respiratory proteins acquired at the origin of Pseudorhizobium are combined with clade-specific genes to encode different strategies for detoxification and nutrition in harsh, nutrient-poor environments. Finally, we predict diagnostic phenotypes for the distinction of P. banfieldiae from other Pseudorhizobium species, including autotrophy and sensitivity to the azo dye Congo Red, which we experimentally validated.

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Automated reconstruction of all gene histories in large bacterial pangenome datasets and search for co-evolved gene modules with Pantagruel

Cited by 15 publications

References 29 publications

Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

Genomic analysis provides novel insights into diversification and taxonomy ofAllorhizobium vitis(i.e.Agrobacterium vitis)

Phylogenomic analysis reveals the basis of adaptation of Pseudorhizobium species to extreme environments

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