Re-evaluating the evidence for a universal genetic boundary among microbial species

Murray, Connor S.; Gao, Yingnan; Wu, Martin

doi:10.1038/s41467-021-24128-2

Cited by 43 publications

(42 citation statements)

References 19 publications

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“…In other words, strains either belong to the same natural biological entity at the species level and have > 95% ANI, or belong to different species and have < 82% ANI. This observation could be due to biases in the sampling of available genomes, or the all-against-all pairwise comparisons included mostly distantly-related species [ 11 ]. In our study that provided a detailed examination of closely related species, the ~ 85–93% ANI among A. tumefaciens genomospecies (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…First, while genomospecies defined by overall genome divergence were suggested to represent distinct biological entities [ 5 – 9 ], the exact criteria for establishing the species boundaries are disputed. Although 95% average nucleotide identity (ANI) across the conserved parts of genomes was proposed as a universal boundary for defining species in bacteria [ 10 ], this criterion was challenged [ 11 ]. Additionally, ANI values alone do not provide information such as gene content or phylogenetic relationships, which are critical in understanding biological entities [ 4 ].…”

Section: Introductionmentioning

confidence: 99%

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Modular evolution of secretion systems and virulence plasmids in a bacterial species complex

et al. 2022

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Background Many named species as defined in current bacterial taxonomy correspond to species complexes. Uncertainties regarding the organization of their genetic diversity challenge research efforts. We utilized the Agrobacterium tumefaciens species complex (a.k.a. Agrobacterium biovar 1), a taxon known for its phytopathogenicity and applications in transformation, as a study system and devised strategies for investigating genome diversity and evolution of species complexes. Results We utilized 35 genome assemblies, including 14 newly generated ones, to achieve a phylogenetically balanced sampling of A. tumefaciens. Our genomic analysis suggested that the 10 genomospecies described previously are distinct biological species and supported a quantitative guideline for species delineation. Furthermore, our inference of gene content and core-genome phylogeny allowed for investigations of genes critical in fitness and ecology. For the type VI secretion system (T6SS) involved in interbacterial competition and thought to be conserved, we detected multiple losses and one horizontal gene transfer. For the tumor-inducing plasmids (pTi) and pTi-encoded type IV secretion system (T4SS) that are essential for agrobacterial phytopathogenicity, we uncovered novel diversity and hypothesized their involvement in shaping this species complex. Intriguingly, for both T6SS and T4SS, genes encoding structural components are highly conserved, whereas extensive diversity exists for genes encoding effectors and other proteins. Conclusions We demonstrate that the combination of a phylogeny-guided sampling scheme and an emphasis on high-quality assemblies provides a cost-effective approach for robust analysis in evolutionary genomics. We show that the T6SS VgrG proteins involved in specific effector binding and delivery can be classified into distinct types based on domain organization. The co-occurrence patterns of VgrG-associated domains and the neighboring genes that encode different chaperones/effectors can be used to infer possible interacting partners. Similarly, the associations between plant host preference and the pTi type among these strains can be used to infer phenotype-genotype correspondence. Our strategies for multi-level investigations at scales that range from whole genomes to intragenic domains and phylogenetic depths from between- to within-species are applicable to other bacteria. Furthermore, modularity observed in the molecular evolution of genes and domains is useful for inferring functional constraints and informing experimental works.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Modular evolution of secretion systems and virulence plasmids in a bacterial species complex

et al. 2022

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“…However, when genome data are compared globally, i.e. not taking strain cohabitation into account, it is not uncommon for pairs of strains to have ANI values between 83% and 95% ( 5 , 34 ).…”

Section: Average Nucleotide Identity For Delineating Speciesmentioning

confidence: 99%

GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy

Parks

Chuvochina

Rinke

et al. 2021

Nucleic Acids Research

966

832

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The Genome Taxonomy Database (GTDB; https://gtdb.ecogenomic.org) provides a phylogenetically consistent and rank normalized genome-based taxonomy for prokaryotic genomes sourced from the NCBI Assembly database. GTDB R06-RS202 spans 254 090 bacterial and 4316 archaeal genomes, a 270% increase since the introduction of the GTDB in November, 2017. These genomes are organized into 45 555 bacterial and 2339 archaeal species clusters which is a 200% increase since the integration of species clusters into the GTDB in June, 2019. Here, we explore prokaryotic diversity from the perspective of the GTDB and highlight the importance of metagenome-assembled genomes in expanding available genomic representation. We also discuss improvements to the GTDB website which allow tracking of taxonomic changes, easy assessment of genome assembly quality, and identification of genomes assembled from type material or used as species representatives. Methodological updates and policy changes made since the inception of the GTDB are then described along with the procedure used to update species clusters in the GTDB. We conclude with a discussion on the use of average nucleotide identities as a pragmatic approach for delineating prokaryotic species.

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“…The authors concluded that a clear genetic discontinuum and species boundary were evident from the unprecedented large-scale ANI analysis and claimed that the 95% ANI threshold represented an accurate threshold for demarcating almost all currently named prokaryotic species. Murray et al [100] argued that the creation of a universal genetic boundary among the named species in the current NCBI taxonomy was questionable and that it resulted from substantially biased sampling in genome sequencing. They urged caution against being excessively confident in using 95% ANI for microbial species delineation, since the high benchmarks reported in the paper were inflated by the use of highly redundant genomes.…”

Section: Challenges Of Curtobacterium Taxonomic Classificationmentioning

confidence: 99%

“…Free living microbes exploring different habitats are more likely to exhibit a genetic continuum. Selection is also unlikely to produce a universal genetic boundary, as microbial species are unique in nature, with each species subject to its own evolutionary and ecological forces [100].…”

Section: Challenges Of Curtobacterium Taxonomic Classificationmentioning

confidence: 99%

Curtobacterium spp. and Curtobacterium flaccumfaciens: Phylogeny, Genomics-Based Taxonomy, Pathogenicity, and Diagnostics

Evseev

Lukianova

Tarakanov

et al. 2022

CIMB

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The genus of Curtobacterium, belonging to the Microbacteriaceae family of the Actinomycetales order, includes economically significant pathogenic bacteria of soybeans and other agricultural crops. Thorough phylogenetic and full-genome analysis using the latest genomic data has demonstrated a complex and contradictory taxonomic picture within the group of organisms classified as the Curtobacterium species. Based on these data, it is possible to delineate about 50 new species and to reclassify a substantial part of the Curtobacterium strains. It is suggested that 53 strains, including most of the Curtobacterium flaccumfaciens pathovars, can compose a monophyletic group classified as C. flaccumfaciens. A genomic analysis using the most recent inventory of bacterial chromosomal and plasmid genomes deposited to GenBank confirmed the possible role of Microbacteriaceae plasmids in pathogenicity and demonstrated the existence of a group of related plasmids carrying virulence factors and possessing a gene distantly related to DNA polymerase found in bacteriophages and archaeal and eukaryotic viruses. A PCR diagnostic assay specific to the genus Curtobacterium was developed and tested. The presented results assist in the understanding of the evolutionary relations within the genus and can lay the foundation for further taxonomic updates.

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Re-evaluating the evidence for a universal genetic boundary among microbial species

Cited by 43 publications

References 19 publications

Modular evolution of secretion systems and virulence plasmids in a bacterial species complex

Modular evolution of secretion systems and virulence plasmids in a bacterial species complex

GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy

Curtobacterium spp. and Curtobacterium flaccumfaciens: Phylogeny, Genomics-Based Taxonomy, Pathogenicity, and Diagnostics

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