Dataset Information

Family-wide Structural Characterization and Genomic Comparisons Decode the Diversity-oriented Biosynthesis of Thalassospiramides by Marine Proteobacteria.

ABSTRACT: The thalassospiramide lipopeptides have great potential for therapeutic applications; however, their structural and functional diversity and biosynthesis are poorly understood. Here, by cultivating 130 Rhodospirillaceae strains sampled from oceans worldwide, we discovered 21 new thalassospiramide analogues and demonstrated their neuroprotective effects. To investigate the diversity of biosynthetic gene cluster (BGC) architectures, we sequenced the draft genomes of 28 Rhodospirillaceae strains. Our family-wide genomic analysis revealed three types of dysfunctional BGCs and four functional BGCs whose architectures correspond to four production patterns. This correlation allowed us to reassess the "diversity-oriented biosynthesis" proposed for the microbial production of thalassospiramides, which involves iteration of several key modules. Preliminary evolutionary investigation suggested that the functional BGCs could have arisen through module/domain loss, whereas the dysfunctional BGCs arose through horizontal gene transfer. Further comparative genomics indicated that thalassospiramide production is likely to be attendant on particular genes/pathways for amino acid metabolism, signaling transduction, and compound efflux. Our findings provide a systematic understanding of thalassospiramide production and new insights into the underlying mechanism.

SUBMITTER: Zhang W

PROVIDER: S-EPMC5207150 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Family-wide Structural Characterization and Genomic Comparisons Decode the Diversity-oriented Biosynthesis of Thalassospiramides by Marine Proteobacteria.

Zhang Weipeng W Lu Liang L Lai Qiliang Q Zhu Beika B Li Zhongrui Z Xu Ying Y Shao Zongze Z Herrup Karl K Moore Bradley S BS Ross Avena C AC Qian Pei-Yuan PY

The Journal of biological chemistry 20161114 53

The thalassospiramide lipopeptides have great potential for therapeutic applications; however, their structural and functional diversity and biosynthesis are poorly understood. Here, by cultivating 130 Rhodospirillaceae strains sampled from oceans worldwide, we discovered 21 new thalassospiramide analogues and demonstrated their neuroprotective effects. To investigate the diversity of biosynthetic gene cluster (BGC) architectures, we sequenced the draft genomes of 28 Rhodospirillaceae strains. O ...[more]

PMID: 27875306

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Project description:Recent changes in the taxonomy of the Pseudomonadaceae family have led to the delineation of three new genera (Atopomonas, Halopseudomonas and Stutzerimonas). However, the genus Pseudomonas remains the most densely populated and displays a broad genetic diversity. Pseudomonas are able to produce a wide variety of secondary metabolites which drives important ecological functions and have a great impact in sustaining their lifestyles. While soilborne Pseudomonas are constantly examined, we currently lack studies aiming to explore the genetic diversity and metabolic potential of marine Pseudomonas spp. In this study, 23 Pseudomonas strains were co-isolated with Vibrio strains from three marine microalgal cultures and rpoD-based phylogeny allowed their assignment to the Pseudomonas oleovorans group (Pseudomonas chengduensis, Pseudomonas toyotomiensis and one new species). We combined whole genome sequencing on three selected strains with an inventory of marine Pseudomonas genomes to assess their phylogenetic assignations and explore their metabolic potential. Our results revealed that most strains are incorrectly assigned at the species level and half of them do not belong to the genus Pseudomonas but instead to the genera Halopseudomonas or Stutzerimonas. We highlight the presence of 26 new species (Halopseudomonas (n = 5), Stutzerimonas (n = 7) and Pseudomonas (n = 14)) and describe one new species, Pseudomonas chaetocerotis sp. nov. (type strain 536T = LMG 31766T = DSM 111343T). We used genome mining to identify numerous BGCs coding for the production of diverse known metabolites (i.e., osmoprotectants, photoprotectants, quorum sensing molecules, siderophores, cyclic lipopeptides) but also unknown metabolites (e.g., ARE, hybrid ARE-DAR, siderophores, orphan NRPS gene clusters) awaiting chemical characterization. Finally, this study underlines that marine environments host a huge diversity of Pseudomonadaceae that can drive the discovery of new secondary metabolites.

Dataset Information

Family-wide Structural Characterization and Genomic Comparisons Decode the Diversity-oriented Biosynthesis of Thalassospiramides by Marine Proteobacteria.

Publications

Family-wide Structural Characterization and Genomic Comparisons Decode the Diversity-oriented Biosynthesis of Thalassospiramides by Marine Proteobacteria.

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