Computational Tools for Discovering and Engineering Natural Product Biosynthetic Pathways

Ren, Hengqian; Shi, Chengyou; Zhao, Huimin

doi:10.1016/j.isci.2019.100795

Title: Computational Tools for Discovering and Engineering Natural Product Biosynthetic Pathways

Abstract

Natural products (NPs), also known as secondary metabolites, are produced in bacteria, fungi, and plants. NPs represent a rich source of antibacterial, antifungal, and anticancer agents. Recent advances in DNA sequencing technologies and bioinformatics unveiled nature’s great potential for synthesizing numerous NPs that may confer unprecedented structural and biological features. However, discovering novel bioactive NPs by genome mining remains a challenge. Moreover, even with interesting bioactivity, the low productivity of many NPs significantly limits their practical applications. Here we discuss the progress in developing bioinformatics tools for efficient discovery of bioactive NPs. In addition, we highlight computational methods for optimizing the productivity of NPs with pharmaceutical importance.

Authors:

Ren, Hengqian; Shi, Chengyou;

Publication Date:: Wed Jan 01 00:00:00 EST 2020

Research Org.:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1581825

Alternate Identifier(s):: OSTI ID: 1581188

Grant/Contract Number:: SC0018420; SC0018260; GM077596; AI144967

Resource Type:: Published Article

Journal Name:: iScience

Additional Journal Information:: Journal Name: iScience Journal Volume: 23 Journal Issue: 1; Journal ID: ISSN 2589-0042

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; biosynthesis; natural products; biosynthetic gene clusters; biosynthetic pathways; synthetic biology

Citation Formats


                    Ren, Hengqian, Shi, Chengyou, and Zhao, Huimin. Computational Tools for Discovering and Engineering Natural Product Biosynthetic Pathways.  Netherlands: N. p., 2020. 
Web.  doi:10.1016/j.isci.2019.100795.

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                    Ren, Hengqian, Shi, Chengyou, & Zhao, Huimin. Computational Tools for Discovering and Engineering Natural Product Biosynthetic Pathways.  Netherlands.  https://doi.org/10.1016/j.isci.2019.100795

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                    Ren, Hengqian, Shi, Chengyou, and Zhao, Huimin. Wed .  
"Computational Tools for Discovering and Engineering Natural Product Biosynthetic Pathways".  Netherlands.  https://doi.org/10.1016/j.isci.2019.100795.

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@article{osti_1581825,

  title        = {Computational Tools for Discovering and Engineering Natural Product Biosynthetic Pathways},

  author       = {Ren, Hengqian and Shi, Chengyou and Zhao, Huimin},

  abstractNote = {Natural products (NPs), also known as secondary metabolites, are produced in bacteria, fungi, and plants. NPs represent a rich source of antibacterial, antifungal, and anticancer agents. Recent advances in DNA sequencing technologies and bioinformatics unveiled nature’s great potential for synthesizing numerous NPs that may confer unprecedented structural and biological features. However, discovering novel bioactive NPs by genome mining remains a challenge. Moreover, even with interesting bioactivity, the low productivity of many NPs significantly limits their practical applications. Here we discuss the progress in developing bioinformatics tools for efficient discovery of bioactive NPs. In addition, we highlight computational methods for optimizing the productivity of NPs with pharmaceutical importance.},

  doi          = {10.1016/j.isci.2019.100795},

  journal      = {iScience},

  number       = 1,

  volume       = 23,

  place        = {Netherlands},

  year         = {Wed Jan 01 00:00:00 EST 2020},

  month        = {Wed Jan 01 00:00:00 EST 2020}

}

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Microbial natural products are a major source of bioactive compounds for drug discovery. Among these molecules, nonribosomal peptides (NRPs) represent a diverse class of natural products that include antibiotics, immunosuppressants, and anticancer agents. Recent breakthroughs in natural product discovery have revealed the chemical structure of several thousand NRPs. However, biosynthetic gene clusters (BGCs) encoding them are known only for a few hundred compounds. Here, we developed Nerpa, a computational method for the high-throughput discovery of novel BGCs responsible for producing known NRPs. After searching 13,399 representative bacterial genomes from the RefSeq repository against 8368 known NRPs, Nerpa linked 117 BGCsmore »« less
https://doi.org/10.3390/metabo11100693
Bioinformatic and Mechanistic Analysis of the Palmerolide PKS-NRPS Biosynthetic Pathway From the Microbiome of an Antarctic Ascidian

Journal Article Avalon, Nicole E. ; Murray, Alison E. ; Daligault, Hajnalka Erzsebet ; ... - Frontiers in Chemistry

Complex interactions exist between microbiomes and their hosts. Increasingly, defensive metabolites that have been attributed to host biosynthetic capability are now being recognized as products of host-associated microbes. These unique metabolites often have bioactivity targets in human disease and can be purposed as pharmaceuticals. Polyketides are a complex family of natural products that often serve as defensive metabolites for competitive or pro-survival purposes for the producing organism, while demonstrating bioactivity in human diseases as cholesterol lowering agents, anti-infectives, and anti-tumor agents. Marine invertebrates and microbes are a rich source of polyketides. Palmerolide A, a polyketide isolated from the Antarctic ascidianmore »« less
https://doi.org/10.3389/fchem.2021.802574

Full Text Available
Plant-derived antifungal agent poacic acid targets β-1,3-glucan

Journal Article Piotrowski, Jeff S. ; Okada, Hiroki ; Lu, Fachuang ; ... - Proceedings of the National Academy of Sciences of the United States of America

A rise in resistance to current antifungals necessitates strategies to identify alternative sources of effective fungicides. We report the discovery of poacic acid, a potent antifungal compound found in lignocellulosic hydrolysates of grasses. Chemical genomics using Saccharomyces cerevisiae showed that loss of cell wall synthesis and maintenance genes conferred increased sensitivity to poacic acid. Morphological analysis revealed that cells treated with poacic acid behaved similarly to cells treated with other cell wall-targeting drugs and mutants with deletions in genes involved in processes related to cell wall biogenesis. Poacic acid causes rapid cell lysis and is synergistic with caspofungin and fluconazole.more »« less
Cited by 71
https://doi.org/10.1073/pnas.1410400112

Full Text Available
Novel soil bacteria possess diverse genes for secondary metabolite biosynthesis

Journal Article Crits-Christoph, Alexander ; Diamond, Spencer ; Butterfield, Cristina N. ; ... - Nature (London)

In soil ecosystems, microorganisms produce diverse secondary metabolites such as antibiotics, antifungals and siderophores that mediate communication, competition and interactions with other organisms and the environment. Most known antibiotics are derived from a few culturable microbial taxa3, and the biosynthetic potential of the vast majority of bacteria in soil has rarely been investigated4. Here we reconstruct hundreds of near-complete genomes from grassland soil metagenomes and identify microorganisms from previously understudied phyla that encode diverse polyketide and nonribosomal peptide biosynthetic gene clusters that are divergent from well-studied clusters. These biosynthetic loci are encoded by newly identified members of the Acidobacteria, Verrucomicobiamore »« less
https://doi.org/10.1038/s41586-018-0207-y

Full Text Available
Exploration of the Biosynthetic Potential of the Populus Microbiome

Journal Article Blair, Patricia M. ; Land, Miriam L. ; Piatek, Marek J. ; ... - mSystems

Natural products (NPs) isolated from bacteria have dramatically advanced human society, especially in medicine and agriculture. The rapidity and ease of genome sequencing have enabled bioinformatics-guided NP discovery and characterization. As a result, NP potential and diversity within a complex community, such as the microbiome of a plant, are rapidly expanding areas of scientific exploration. Here, we assess biosynthetic diversity in the Populus microbiome by analyzing both bacterial isolate genomes and metagenome samples. We utilize the fully sequenced genomes of isolates from the Populus root microbiome to characterize a subset of organisms for NP potential. The more than 3,400 individualmore »« less
Cited by 29
https://doi.org/10.1128/mSystems.00045-18

Full Text Available

Similar Records

Title: Computational Tools for Discovering and Engineering Natural Product Biosynthetic Pathways

Abstract

Citation Formats

Antibiotic resistance–mediated isolation of scaffold-specific natural product producers journal, May 2014

A review of computational tools for design and reconstruction of metabolic pathways journal, December 2017

PRISM 3: expanded prediction of natural product chemical structures from microbial genomes journal, April 2017

Identification of Thiotetronic Acid Antibiotic Biosynthetic Pathways by Target-directed Genome Mining journal, October 2015

Predicting synonymous codon usage and optimizing the heterologous gene for expression in E. coli journal, August 2017

The antiSMASH database version 2: a comprehensive resource on secondary metabolite biosynthetic gene clusters journal, November 2018

Data access for the 1,000 Plants (1KP) project journal, October 2014

KEGG: Kyoto Encyclopedia of Genes and Genomes journal, January 2000

A New Golden Age of Natural Products Drug Discovery journal, December 2015

Computational tools for enzyme improvement: why everyone can – and should – use them journal, April 2017

WGCNA: an R package for weighted correlation network analysis journal, December 2008

CLUSEAN: A computer-based framework for the automated analysis of bacterial secondary metabolite biosynthetic gene clusters journal, March 2009

Complete biosynthesis of cannabinoids and their unnatural analogues in yeast journal, February 2019

TATA is a modular component of synthetic promoters journal, July 2010

OPTIMIZER: a web server for optimizing the codon usage of DNA sequences journal, May 2007

SMURF: Genomic mapping of fungal secondary metabolite clusters journal, September 2010

Discovery of microbial natural products by activation of silent biosynthetic gene clusters journal, June 2015

An introduction to the medicinal plant genome project journal, June 2011

JCat: a novel tool to adapt codon usage of a target gene to its potential expression host journal, July 2005

antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences journal, June 2011

Natural Products as Sources of New Drugs from 1981 to 2014 journal, October 2015

antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification journal, April 2017

Direct cloning of large genomic sequences journal, May 2012

Visual gene developer: a fully programmable bioinformatics software for synthetic gene optimization journal, August 2011

“CodonWizard” – An intuitive software tool with graphical user interface for customizable codon optimization in protein expression efforts journal, August 2019

Assembly-Line Enzymology for Polyketide and Nonribosomal Peptide Antibiotics: Logic, Machinery, and Mechanisms journal, August 2006

MIBiG 2.0: a repository for biosynthetic gene clusters of known function journal, October 2019

Automated genome mining for natural products journal, January 2009

Phylogenomic Analysis of Natural Products Biosynthetic Gene Clusters Allows Discovery of Arseno-Organic Metabolites in Model Streptomycetes journal, June 2016

Design of computational retrobiosynthesis tools for the design of de novo synthetic pathways journal, October 2015

CoExpNetViz: Comparative Co-Expression Networks Construction and Visualization Tool journal, January 2016

De novo design of bioactive protein switches journal, July 2019

A Review of the Microbial Production of Bioactive Natural Products and Biologics journal, June 2019

Computational codon optimization of synthetic gene for protein expression journal, January 2012

Natural products against Alzheimer's disease: Pharmaco-therapeutics and biotechnological interventions journal, March 2017

Presyncodon, a Web Server for Gene Design with the Evolutionary Information of the Expression Hosts journal, December 2018

Computer-aided re-engineering of nonribosomal peptide and polyketide biosynthetic assembly lines journal, January 2019

Codon Bias as a Means to Fine-Tune Gene Expression journal, July 2015

Insights into Secondary Metabolism from a Global Analysis of Prokaryotic Biosynthetic Gene Clusters journal, July 2014

Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes journal, August 2005

ClustScan : an integrated program package for the semi-automatic annotation of modular biosynthetic gene clusters and in silico prediction of novel chemical structures journal, October 2008

antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters journal, May 2015

Complete biosynthesis of opioids in yeast journal, August 2015

BacPP: Bacterial promoter prediction—A tool for accurate sigma-factor specific assignment in enterobacteria journal, October 2011

Using RNA Sequence and Structure for the Prediction of Riboswitch Aptamer: A Comprehensive Review of Available Software and Tools journal, January 2018

EvoMining reveals the origin and fate of natural product biosynthetic enzymes journal, December 2019

Synthetic biology strategies for microbial biosynthesis of plant natural products journal, May 2019

RetroPath2.0: A retrosynthesis workflow for metabolic engineers journal, January 2018

Synthetic promoter libraries – tuning of gene expression journal, February 2006

RibEx: a web server for locating riboswitches and other conserved bacterial regulatory elements journal, July 2005

Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles 1 1Edited by J. Doudna journal, November 2001

The Antibiotic Resistant Target Seeker (ARTS), an exploration engine for antibiotic cluster prioritization and novel drug target discovery journal, May 2017

Defining and combating antibiotic resistance from One Health and Global Health perspectives journal, August 2019

Improving heterologous membrane protein production in Escherichia coli by combining transcriptional tuning and codon usage algorithms journal, September 2017

eSNaPD: A Versatile, Web-Based Bioinformatics Platform for Surveying and Mining Natural Product Biosynthetic Diversity from Metagenomes journal, August 2014

COStar: A D-star Lite-based dynamic search algorithm for codon optimization journal, March 2014

Advances in protein structure prediction and design journal, August 2019

A high-throughput screening and computation platform for identifying synthetic promoters with enhanced cell-state specificity (SPECS) journal, June 2019

Evolution of the Cannabinoid and Terpene Content during the Growth of Cannabis sativa Plants from Different Chemotypes journal, January 2016

BAGEL3: automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides journal, May 2013

The Eukaryotic Promoter Database: expansion of EPDnew and new promoter analysis tools journal, November 2014

A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence journal, September 2015

GeMS: an advanced software package for designing synthetic genes journal, May 2005

Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources journal, April 2014

Synthetic biology to access and expand nature's chemical diversity journal, February 2016

antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers journal, May 2013

WebGeSTer DB—a transcription terminator database journal, November 2010

Efficient search, mapping, and optimization of multi-protein genetic systems in diverse bacteria journal, June 2014

Modular and tunable biological feedback control using a de novo protein switch journal, July 2019

The Natural Product Domain Seeker NaPDoS: A Phylogeny Based Bioinformatic Tool to Classify Secondary Metabolite Gene Diversity journal, March 2012

Codon and Codon-Pair Usage Tables (CoCoPUTs): Facilitating Genetic Variation Analyses and Recombinant Gene Design journal, June 2019

Rationally reduced libraries for combinatorial pathway optimization minimizing experimental effort journal, March 2016

Machine-learning-guided directed evolution for protein engineering journal, July 2019

Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites journal, November 2013

plantiSMASH: automated identification, annotation and expression analysis of plant biosynthetic gene clusters journal, April 2017

UpGene: Application of a Web-Based DNA Codon Optimization Algorithm journal, January 2004

SBSPKS: structure based sequence analysis of polyketide synthases journal, May 2010

Antibiotic resistance–mediated isolation of scaffold-specific natural product producers
journal, May 2014

A review of computational tools for design and reconstruction of metabolic pathways
journal, December 2017

PRISM 3: expanded prediction of natural product chemical structures from microbial genomes
journal, April 2017

Identification of Thiotetronic Acid Antibiotic Biosynthetic Pathways by Target-directed Genome Mining
journal, October 2015

Predicting synonymous codon usage and optimizing the heterologous gene for expression in E. coli
journal, August 2017

The antiSMASH database version 2: a comprehensive resource on secondary metabolite biosynthetic gene clusters
journal, November 2018

Data access for the 1,000 Plants (1KP) project
journal, October 2014

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

A New Golden Age of Natural Products Drug Discovery
journal, December 2015

Computational tools for enzyme improvement: why everyone can – and should – use them
journal, April 2017

WGCNA: an R package for weighted correlation network analysis
journal, December 2008

CLUSEAN: A computer-based framework for the automated analysis of bacterial secondary metabolite biosynthetic gene clusters
journal, March 2009

Complete biosynthesis of cannabinoids and their unnatural analogues in yeast
journal, February 2019

TATA is a modular component of synthetic promoters
journal, July 2010

OPTIMIZER: a web server for optimizing the codon usage of DNA sequences
journal, May 2007

SMURF: Genomic mapping of fungal secondary metabolite clusters
journal, September 2010

Discovery of microbial natural products by activation of silent biosynthetic gene clusters
journal, June 2015

An introduction to the medicinal plant genome project
journal, June 2011

JCat: a novel tool to adapt codon usage of a target gene to its potential expression host
journal, July 2005

antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences
journal, June 2011

Natural Products as Sources of New Drugs from 1981 to 2014
journal, October 2015

antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification
journal, April 2017

Direct cloning of large genomic sequences
journal, May 2012

Visual gene developer: a fully programmable bioinformatics software for synthetic gene optimization
journal, August 2011

“CodonWizard” – An intuitive software tool with graphical user interface for customizable codon optimization in protein expression efforts
journal, August 2019

Assembly-Line Enzymology for Polyketide and Nonribosomal Peptide Antibiotics: Logic, Machinery, and Mechanisms
journal, August 2006

MIBiG 2.0: a repository for biosynthetic gene clusters of known function
journal, October 2019

Automated genome mining for natural products
journal, January 2009

Phylogenomic Analysis of Natural Products Biosynthetic Gene Clusters Allows Discovery of Arseno-Organic Metabolites in Model Streptomycetes
journal, June 2016

Design of computational retrobiosynthesis tools for the design of de novo synthetic pathways
journal, October 2015

CoExpNetViz: Comparative Co-Expression Networks Construction and Visualization Tool
journal, January 2016

De novo design of bioactive protein switches
journal, July 2019

A Review of the Microbial Production of Bioactive Natural Products and Biologics
journal, June 2019

Computational codon optimization of synthetic gene for protein expression
journal, January 2012

Natural products against Alzheimer's disease: Pharmaco-therapeutics and biotechnological interventions
journal, March 2017

Presyncodon, a Web Server for Gene Design with the Evolutionary Information of the Expression Hosts
journal, December 2018

Computer-aided re-engineering of nonribosomal peptide and polyketide biosynthetic assembly lines
journal, January 2019

Codon Bias as a Means to Fine-Tune Gene Expression
journal, July 2015

Insights into Secondary Metabolism from a Global Analysis of Prokaryotic Biosynthetic Gene Clusters
journal, July 2014

Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes
journal, August 2005

ClustScan : an integrated program package for the semi-automatic annotation of modular biosynthetic gene clusters and in silico prediction of novel chemical structures
journal, October 2008

antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters
journal, May 2015

Complete biosynthesis of opioids in yeast
journal, August 2015

BacPP: Bacterial promoter prediction—A tool for accurate sigma-factor specific assignment in enterobacteria
journal, October 2011

Using RNA Sequence and Structure for the Prediction of Riboswitch Aptamer: A Comprehensive Review of Available Software and Tools
journal, January 2018

EvoMining reveals the origin and fate of natural product biosynthetic enzymes
journal, December 2019

Synthetic biology strategies for microbial biosynthesis of plant natural products
journal, May 2019

RetroPath2.0: A retrosynthesis workflow for metabolic engineers
journal, January 2018

Synthetic promoter libraries – tuning of gene expression
journal, February 2006

RibEx: a web server for locating riboswitches and other conserved bacterial regulatory elements
journal, July 2005

Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles 1 1Edited by J. Doudna
journal, November 2001

The Antibiotic Resistant Target Seeker (ARTS), an exploration engine for antibiotic cluster prioritization and novel drug target discovery
journal, May 2017

Defining and combating antibiotic resistance from One Health and Global Health perspectives
journal, August 2019

Improving heterologous membrane protein production in Escherichia coli by combining transcriptional tuning and codon usage algorithms
journal, September 2017

eSNaPD: A Versatile, Web-Based Bioinformatics Platform for Surveying and Mining Natural Product Biosynthetic Diversity from Metagenomes
journal, August 2014

COStar: A D-star Lite-based dynamic search algorithm for codon optimization
journal, March 2014

Advances in protein structure prediction and design
journal, August 2019

A high-throughput screening and computation platform for identifying synthetic promoters with enhanced cell-state specificity (SPECS)
journal, June 2019

Evolution of the Cannabinoid and Terpene Content during the Growth of Cannabis sativa Plants from Different Chemotypes
journal, January 2016

BAGEL3: automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides
journal, May 2013

The Eukaryotic Promoter Database: expansion of EPDnew and new promoter analysis tools
journal, November 2014

A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence
journal, September 2015

GeMS: an advanced software package for designing synthetic genes
journal, May 2005

Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources
journal, April 2014

Synthetic biology to access and expand nature's chemical diversity
journal, February 2016

antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers
journal, May 2013

WebGeSTer DB—a transcription terminator database
journal, November 2010

Efficient search, mapping, and optimization of multi-protein genetic systems in diverse bacteria
journal, June 2014

Modular and tunable biological feedback control using a de novo protein switch
journal, July 2019

The Natural Product Domain Seeker NaPDoS: A Phylogeny Based Bioinformatic Tool to Classify Secondary Metabolite Gene Diversity
journal, March 2012

Codon and Codon-Pair Usage Tables (CoCoPUTs): Facilitating Genetic Variation Analyses and Recombinant Gene Design
journal, June 2019

Rationally reduced libraries for combinatorial pathway optimization minimizing experimental effort
journal, March 2016

Machine-learning-guided directed evolution for protein engineering
journal, July 2019

Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites
journal, November 2013

plantiSMASH: automated identification, annotation and expression analysis of plant biosynthetic gene clusters
journal, April 2017

UpGene: Application of a Web-Based DNA Codon Optimization Algorithm
journal, January 2004

SBSPKS: structure based sequence analysis of polyketide synthases
journal, May 2010

Automated design of synthetic ribosome binding sites to control protein expression
journal, October 2009

A new genome-mining tool redefines the lasso peptide biosynthetic landscape
journal, February 2017

High Guanine and Cytosine Content Increases mRNA Levels in Mammalian Cells
journal, May 2006