Horizontal Gene Transfer and Genome Evolution in the Phylum Actinobacteria

Park, Cooper J.; Smith, Joshua T.; Andam, Cheryl P.

doi:10.1007/978-3-030-21862-1_5

Cited by 11 publications

(11 citation statements)

References 137 publications

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“…Prior analyses of Salinispora BGCs revealed extensive horizontal gene transfer (HGT) and exchange both within and between species (19), suggesting a “plug and play” model of BGC evolution (20). These observations are consistent with the prevailing view in natural product research that BGCs are rapidly gained and lost via HGT (21-23), particularly within Actinobacteria taxa (24). In Salinispora , the exchange of BGCs between species is likely mediated by conjugative elements, as in Streptomyces (25), and further facilitated by the absence of geographic barriers in their distribution (26).…”

supporting

confidence: 91%

“…Similarly, we observed a distinct phylogenetic signal at both the BGC ( Figure 2) and metabolite levels ( Figure 3A), indicating that vertical inheritance is a major driver of BGC evolution. While horizontal gene transfer (HGT) may play a major role in expanding BGC diversity, the prevailing view that BGCs are rapidly gained and lost (46)(47)(48)(49) remains difficult to discern given that genomic signatures (e.g., GC% and tetranucleotide bias) can be lost over time (50). As such, the time scales in which these events occur are highly relevant when considering the processes driving BGC evolution.…”

Section: Discussionmentioning

confidence: 99%

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Vertical inheritance governs biosynthetic gene cluster evolution and chemical diversification

Chase

Sweeney

Muskat

et al. 2020

Preprint

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While specialized metabolites are thought to mediate ecological interactions, the evolutionary processes driving their distributions, particularly among closely related lineages, remain poorly understood. Here, we examine the evolutionary dynamics governing the diversity and distribution of biosynthetic gene clusters (BGCs) in 118 strains across nine described species within the marine actinomycete genus Salinispora. While previous evidence indicated that horizontal gene transfer largely contributed to BGC diversity, we find that a majority of BGCs in Salinispora genomes are maintained by processes of vertical descent. In particular, we identified species-specific signatures that were associated with both BGC distributions and the production of their encoded specialized metabolites. By analyzing nine experimentally characterized BGCs that range in conservation from species to genus specific, we find that the distribution of BGCs among Salinispora species is maintained by selection, while BGC diversification is constrained by recombination among closely related strains and strengthened by gain/loss events between species. Notably, the evolutionary processes driving BGC diversification had direct consequences for compound production, elucidating the mechanisms that lead to chemical diversification. These results support the concept that specialized metabolites, and their cognate BGCs, represent functional traits associated with ecological differentiation among Salinispora species.GRAPHICAL ABSTRACT

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supporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Vertical inheritance governs biosynthetic gene cluster evolution and chemical diversification

Chase

Sweeney

Muskat

et al. 2020

Preprint

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“…Yet, the Salinispora spt phylogeny is incongruent with the established species phylogeny ( Figs 5a and S4). These incongruencies are likely due to horizontal gene transfer events, which have been identified as important avenues of BGC transfer and diversification, especially in Actinobacteria [ 100 ]. The most apparent of these events is represented by the clustering of the Salinispora tropica Spt9 sequences within the Salinispora arenicola clade.…”

Section: Discussionmentioning

confidence: 99%

“…It remains unknown whether the Salinispora arenicola spt locus that appears to have replaced the ancestral version or been acquired de novo in Salinispora tropica provides a selective advantage or affects the compounds produced. The apparent interspecies exchange of spt adds to growing evidence that this process occurs between both closely and distantly related bacteria, as seen in the granaticin, coronafacoyl phytotoxins, tunicamycin, foxicin, antimycin, streptomycin and bicyclomycin BGCs [ 100 ]. Overall, acquisition of the spt BGC by Salinispora tropica highlights the importance of understanding the functional roles of its products and the effects of these exchange events on population and species-level dynamics.…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic analysis of the salinipostin γ-butyrolactone gene cluster uncovers new potential for bacterial signalling-molecule diversity

et al. 2021

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Bacteria communicate by small-molecule chemicals that facilitate intra- and inter-species interactions. These extracellular signalling molecules mediate diverse processes including virulence, bioluminescence, biofilm formation, motility and specialized metabolism. The signalling molecules produced by members of the phylum Actinobacteria generally comprise γ-butyrolactones, γ-butenolides and furans. The best-known actinomycete γ-butyrolactone is A-factor, which triggers specialized metabolism and morphological differentiation in the genus Streptomyces . Salinipostins A–K are unique γ-butyrolactone molecules with rare phosphotriester moieties that were recently characterized from the marine actinomycete genus Salinispora . The production of these compounds has been linked to the nine-gene biosynthetic gene cluster (BGC) spt. Critical to salinipostin assembly is the γ-butyrolactone synthase encoded by spt9. Here, we report the surprising distribution of spt9 homologues across 12 bacterial phyla, the majority of which are not known to produce γ-butyrolactones. Further analyses uncovered a large group of spt-like gene clusters outside of the genus Salinispora , suggesting the production of new salinipostin-like diversity. These gene clusters show evidence of horizontal transfer and location-specific recombination among Salinispora strains. The results suggest that γ-butyrolactone production may be more widespread than previously recognized. The identification of new γ-butyrolactone BGCs is the first step towards understanding the regulatory roles of the encoded small molecules in Actinobacteria.

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“…This suggests that the perceived GCF richness in those species was largely confounded by the effect of (multiple) gene insertions/deletions near BGCs (in flanking regions included by antiSMASH)rather than the actual recruitment of new BGCs (i.e. via lateral gene transfer[103][104][105]).…”

mentioning

confidence: 99%

BiG-SLiCE: A Highly Scalable Tool Maps the Diversity of 1.2 Million Biosynthetic Gene Clusters

Kautsar

Hooft

Ridder

et al. 2020

Preprint

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Genome mining for Biosynthetic Gene Clusters (BGCs) has become an integral part of natural product discovery. The >200,000 microbial genomes now publicly available hold information on abundant novel chemistry. One way to navigate this vast genomic diversity is through comparative analysis of homologous BGCs, which allows identification of cross-species patterns that can be matched to the presence of metabolites or biological activities. However, current tools suffer from a bottleneck caused by the expensive network-based approach used to group these BGCs into Gene Cluster Families (GCFs). Here, we introduce BiG-SLiCE, a tool designed to cluster massive numbers of BGCs. By representing them in Euclidean space, BiG-SLiCE can group BGCs into GCFs in a non-pairwise, near-linear fashion. We used BiG-SLiCE to analyze 1,225,071 BGCs collected from 209,206 publicly available microbial genomes and metagenome-assembled genomes (MAGs) within ten days on a typical 36-cores CPU server. We demonstrate the utility of such analyses by reconstructing a global map of secondary metabolic diversity across taxonomy to identify uncharted biosynthetic potential. BiG-SLiCE also provides a "query mode" that can efficiently place newly sequenced BGCs into previously computed GCFs, plus a powerful output visualization engine that facilitates user-friendly data exploration. BiG-SLiCE opens up new possibilities to accelerate natural product discovery and offers a first step towards constructing a global, searchable interconnected network of BGCs. As more genomes get sequenced from understudied taxa, more information can be mined to highlight their potentially novel chemistry. BiG-SLiCE is available via https://github.com/medema-lab/bigslice.

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Horizontal Gene Transfer and Genome Evolution in the Phylum Actinobacteria

Cited by 11 publications

References 137 publications

Vertical inheritance governs biosynthetic gene cluster evolution and chemical diversification

Vertical inheritance governs biosynthetic gene cluster evolution and chemical diversification

Phylogenetic analysis of the salinipostin γ-butyrolactone gene cluster uncovers new potential for bacterial signalling-molecule diversity

BiG-SLiCE: A Highly Scalable Tool Maps the Diversity of 1.2 Million Biosynthetic Gene Clusters

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