Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus<i>Streptomyces</i>

McDonald, Bradon R.; Currie, Cameron R.

doi:10.1128/mbio.00644-17

Cited by 104 publications

(104 citation statements)

References 67 publications

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“…Metagenomic analyses have shown that such gifted actinobacteria are a feature of natural habitats [57,58]. Creative cultivation techniques are available for the isolation of rare and novel actinobacteria with large genomes [27,59], though there is a need to marry innovative selective isolation procedures with the ecology of target organisms [60][61][62][63], as demonstrated by adaptations shown by Salinispora and Streptomyces strains [64,65]. There is also a need to obtain complete genome sequences from especially gifted actinobacteria [33,34] for systematic genome mining for new molecules.…”

Section: Genome Analysismentioning

confidence: 99%

Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 m of bioprospecting campaigns

Bull

Goodfellow

2019

Microbiology

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The rationale of our bioprospecting campaigns is that the extremobiosphere, particularly the deep sea and hyper-arid deserts, harbours undiscovered biodiversity that is likely to express novel chemistry and biocatalysts thereby providing opportunities for therapeutic drug and industrial process development. We have focused on actinobacteria because of their frequent role as keystone species in soil ecosystems and their unrivalled track record as a source of bioactive compounds. Population numbers and diversity of actinobacteria in the extremobiosphere are traditionally considered to be low, although they often comprise the dominant bacterial biota. Recent metagenomic evaluation of 'the uncultured microbial majority' has now revealed enormous taxonomic diversity among 'dark' and 'rare' actinobacteria in samples as diverse as sediments from the depths of the Mariana Trench and soils from the heights of the Central Andes. The application of innovative culture and screening options that emphasize rigorous dereplication at each stage of the analysis, and strain prioritization to identify 'gifted' organisms, have been deployed to detect and characterize bioactive hit compounds and sought-after catalysts from this hitherto untapped resource. The rewards include first-in-a-class chemical entities with novel modes of action, as well as a growing microbial seed bank that represents a potentially enormous source of biotechnological and therapeutic innovation.

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Section: Genome Analysismentioning

confidence: 99%

Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 m of bioprospecting campaigns

Bull

Goodfellow

2019

Microbiology

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“…It is within these arm regions that most of the specialized metabolic clusters are found. Recent work has 47 revealed that specialized metabolic clusters are over-represented as horizontally-transferred elements 48 in the streptomycetes (McDonald and Currie, 2017), and that in the closely-related Salinospora, lateral 49 gene transfer is a major driver of specialized metabolism (Ziemert et al, 2014). 50…”

Section: Introduction 13mentioning

confidence: 99%

Silencing cryptic specialized metabolism inStreptomycesby the nucleoid-associated protein Lsr2

Gehrke

Zhang

Pimentel‐Elardo

et al. 2019

Preprint

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1Lsr2 is a nucleoid-associated protein conserved throughout the actinobacteria, including the antibiotic-2 producing Streptomyces. Streptomyces species encode paralogous Lsr2 proteins or 3 LsrL), and we show here that of the two, Lsr2 has greater functional significance. We found that Lsr2 4 binds AT-rich sequences throughout the chromosome, and broadly represses gene expression. 5 Strikingly, specialized metabolic clusters were over-represented amongst its targets, and the cryptic 6 nature of many of these clusters appears to stem from Lsr2-mediated repression. Manipulating Lsr2 7 activity in model species and uncharacterized isolates resulted in the production of new metabolites not 8 seen in wild type strains. Our results suggest that the transcriptional silencing of biosynthetic clusters by 9Lsr2 may protect Streptomyces from the inappropriate expression of specialized metabolites, and 10 provide global control over Streptomyces' arsenal of signalling and antagonistic compounds. 11 12 Interestingly, however, most clusters are poorly expressed under normal laboratory conditions, and in 54 many cases their associated metabolites remain uncharacterized. This is also the case for the 55 filamentous fungi, many of whom have a broad, untapped specialized metabolic repertoire, courtesy of 56 transcriptional silencing by histones (Pfannenstiel and Keller, 2019). Significant efforts are being made to 57 stimulate the production of these 'cryptic' metabolites in both bacteria and fungi, as they are widely 58 regarded as productive sources of new natural products (Craney et al., 2013;Ochi and Hosaka, 2013; 59 Scharf and Brakhage, 2013;Yoon and Nodwell, 2014; Daniel-Ivad et al., 2017;Onaka, 2017). 60We sought to investigate the role of the nucleoid-associated proteins Lsr2 and LsrL in gene 61 regulation in Streptomyces. We found that deleting lsr2 from the chromosome of Streptomyces 62 venezuelae had minor effects on S. venezuelae growth and development and major effects on 63 metabolism. In contrast, deleting lsrL had no detectable impact on development, and only a minor effect 64 on metabolism. Focussing on Lsr2, we determined that it bound AT-rich regions, generally repressed the 65 expression of prophage genes and other genes unique to S. venezuelae (presumably acquired by lateral 66 gene transfer), and suppressed antisense gene expression. The most profound effect of lsr2 deletion, 67 however, was the large-scale activation of specialized metabolic cluster gene expression. Lsr2 directly 68 repressed the transcription of many cryptic clusters in a way that is analogous to Lsr2-and H-NS-69 mediated repression of pathogenicity islands in other bacteria, and histone-mediated cluster silencing in 70 fungi. Unexpectedly, Lsr2 also controlled the expression of well-characterized and highly-conserved 71 clusters, suggesting that Lsr2 control has been broadly integrated into the regulatory cascades governing 72 specialized metabolism. Our results suggest that Lsr2 functions as a metabolic gatekeeper in the 73 strepto...

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“…The microbial expansin phylogeny indicates that HGT has been an important process shaping the distribution of expansins among microorganisms, and that expansin gene exchange is ongoing. In some cases, the presence of expansin genes in most sequenced species within a group (such as Myxobacteria, Xanthomonadaceae, and the Pectobacterium and Dickeya group of Entobacterial plant pathogens) suggests that original acquisition of an expansin likely occurred in a common ancestor of these taxa before these groups diversified (105). In other species – notably several plant pathogens – acquisition of an expansin likely occurred on more recent ecological time scales.…”

Section: Discussionmentioning

confidence: 99%

From morphogenesis to pathogenesis: A cellulose loosening protein is one of the most widely distributed tools in nature

Chase

Zhaxybayeva

Rocha

et al. 2019

Preprint

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31 Plants must rearrange the network of complex carbohydrates in their cell walls during normal 32 growth and development. To accomplish this, all plants depend on proteins called expansins that 33 non-enzymatically loosen hydrogen bonds between cellulose microfibrils. Because of their key 34 role in cell wall extension during growth, expansin genes are ubiquitous, diverse, and abundant 35 throughout all land plants. Surprisingly, expansin genes have more recently been found in some 36 bacteria and microbial eukaryotes, where their biological functions are largely unknown. Here, 37we reconstruct the phylogeny of microbial expansin genes. We find these genes in all eukaryotic 38 microorganisms that have structural cellulose in their cell walls, suggesting expansins evolved in 39 ancient marine microorganisms long before the evolution of land plants. We also find expansins 40 in an unexpectedly high phylogenetic diversity of bacteria and fungi that do not have cellulosic 41 cell walls. These bacteria and fungi with expansin genes inhabit varied ecological contexts 42 mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell 43 walls are present.

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Lateral Gene Transfer Dynamics in the Ancient Bacterial GenusStreptomyces

Cited by 104 publications

References 67 publications

Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 m of bioprospecting campaigns

Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 m of bioprospecting campaigns

Silencing cryptic specialized metabolism inStreptomycesby the nucleoid-associated protein Lsr2

From morphogenesis to pathogenesis: A cellulose loosening protein is one of the most widely distributed tools in nature

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