ProCarDB: a database of bacterial carotenoids
- L. N. U. Nupur†1,
- Asheema Vats†2,
- Sandeep Kumar Dhanda3,
- Gajendra P. S. Raghava3,
- Anil Kumar Pinnaka4Email author and
- Ashwani Kumar5Email author
© The Author(s). 2016
Received: 28 December 2015
Accepted: 19 May 2016
Published: 26 May 2016
Carotenoids have important functions in bacteria, ranging from harvesting light energy to neutralizing oxidants and acting as virulence factors. However, information pertaining to the carotenoids is scattered throughout the literature. Furthermore, information about the genes/proteins involved in the biosynthesis of carotenoids has tremendously increased in the post-genomic era. A web server providing the information about microbial carotenoids in a structured manner is required and will be a valuable resource for the scientific community working with microbial carotenoids.
Here, we have created a manually curated, open access, comprehensive compilation of bacterial carotenoids named as ProCarDB- Prokaryotic Carotenoid Database. ProCarDB includes 304 unique carotenoids arising from 50 biosynthetic pathways distributed among 611 prokaryotes. ProCarDB provides important information on carotenoids, such as 2D and 3D structures, molecular weight, molecular formula, SMILES, InChI, InChIKey, IUPAC name, KEGG Id, PubChem Id, and ChEBI Id. The database also provides NMR data, UV-vis absorption data, IR data, MS data and HPLC data that play key roles in the identification of carotenoids. An important feature of this database is the extension of biosynthetic pathways from the literature and through the presence of the genes/enzymes in different organisms. The information contained in the database was mined from published literature and databases such as KEGG, PubChem, ChEBI, LipidBank, LPSN, and Uniprot. The database integrates user-friendly browsing and searching with carotenoid analysis tools to help the user. We believe that this database will serve as a major information centre for researchers working on bacterial carotenoids.
KeywordsCarotenoids Carotenoid database ProCarDB Carotenoid biosynthesis pathways Genes encoding for carotenoid biosynthesis Applications of carotenoids Identification of carotenoids
Carotenoids are the isoprenoid derivatives that are characterized by the presence of eight isoprenoids (C5) with a characteristic polyene chain of conjugated double bonds (CDB). The CDB result in distinguishing absorption patterns and are responsible for imparting colours and antioxidant activity to carotenoids . Carotenoids are found in all the photosynthetic organisms as well as in a variety of non-photosynthetic organisms . They perform a variety of functions, ranging from harvesting solar-energy [3, 4] to serve as antioxidants [5, 6] to radio-resistance  and as virulence factors in several pathogens [8–10]. Carotenoids are also known for modulating immune system , scavenging free-radicals , protection from UV radiations, Pro-vitamin A activity and other beneficial properties [13–15] and thus are exploited for the pharmaceutical purposes in many diseases as well as for the health maintenance. Lycopene, β-carotene, canthaxanthin, zeaxanthin and astaxanthin are commercially exploited by nutraceutical industry. Their importance as nutraceuticals is due to their cancer-preventive capabilities [16–20], regulation of lipid metabolism , antioxidant function , obesity prevention [23, 24], and increased longevity . They are used in food products, cosmetics, vitamin supplements, health products as well as feed additives for poultry, livestock, fish and crustaceans . The current demand for carotenoids as dietary supplements is estimated to be worth more than $1.2 billion (http://www.bccresearch.com/market-research/food-and-beverage/carotenoids-global-market-fod025d.html). These supplements are required because human and other animals cannot synthesize carotenoids and therefore, must acquire them through the diet. Their pharmacological importance is primarily attributed to their anti-cancerous/cancer preventive activity [18, 27, 28], anti-diabetic properties [16, 29] and the prevention of cardiovascular diseases though their roles as antioxidants [30, 31]. Given the diverse roles played by these carotenoids, the attention has been focused on the identification and isolation of microbes producing carotenoids and their biosynthetic pathways. Recent efforts have dissected the genetic pathways involved in the synthesis of carotenoids [32–34]. Understanding these pathways at the molecular level has allowed the use of genetic engineering approaches for the biosynthesis of known and novel carotenoids in model microbial strains [32, 35–37]. The knowledge of metabolic engineering and genetic engineering has been strengthened from the high demand for carotenoids as dietary supplements .
The literature reveals a vast body of information on different aspects of carotenoids, such as the abundance of microbial carotenoids, their chemical properties, methods of their characterization, the genetic networks that synchronize carotenoid synthesis, the metabolic pathways involved in the carotenoid biosynthesis, their pharmacological properties and other relevant applications. Despite the availability of this huge amount of information, a unique portal providing all the information at one place has been lacking. Some databases providing limited information on carotenoid consumption in European countries  or the carotenoid content in food  does exist. However, these databases lack information on microbial carotenoids and provide information on specific aspects of carotenoids in the food. In addition to these databases, information on carotenoids can be extracted from LipidBank (http://LipidBank.jp/) and PubChem (https://pubchem.ncbi.nlm.nih.gov/), and information on the pathways involved in carotenoid metabolism can be gathered from the Kyoto Encyclopedia of Genes and Genomes (KEGG, http://www.genome.jp/kegg/).
In the light of renewed interest in microbial carotenoids and the amount of information available on carotenoids, here we have created a user friendly database named ProCarDB (http://bioinfo.imtech.res.in/servers/procardb/) that organizes and provides all the information pertaining to identification, characterization and biosynthesis of carotenoids at one site.
Construction and content
Source of data
The data for ProCarDB were mined from the published literature and various databases. The keywords used for the literature search were “carotenoid,” “microbial carotenoid”, “bacterial carotenoids”, “pigmented bacteria”, and “prokaryotic carotenoid” on various data search platforms, including Pubmed, Google Scholar, International Journal of Systematic and Evolutionary Microbiology (IJSEM), Science Direct and Springer links. We have also consulted books such as Bergey’s Manual of Systematic Bacteriology (2nd edition, Bergey’s Manual Trust), Photosynthesis (J. Amesz, volume 15, 1987, published by Elsevier), Anoxygenic Photosynthetic Bacteria (R.E. Blankenship, M.T. Madigan, C.E. Bauer, 1995, Kluwer Academic Publishers), The Photochemistry of Carotenoids (H.A. Frank et al., 2004, Kluwer Academic Publishers) and Purple Phototrophic Bacteria (C.N. Hunter, F. Daldal, M.C. Thurnauer, J.T. Beatty, 2009, Springer) for harvesting the relevant information on carotenoids. The carotenoid data, such as structure, molecular formula, molecular weight, IUPAC name, InChI, SMILES, UV Spectra, NMR Spectra, and HPLC data were primarily compiled from original manuscripts published or from LipidBank . We have also retrieved information from databases such as PubChem (https://pubchem.ncbi.nlm.nih.gov/), Chemical Entities of Biological Interest (ChEBI, www.ebi.ac.uk/chebi), LipidBank (http://LipidBank.jp/), chemspider (www.chemspider.com/), KEGG (http://www.genome.jp/kegg/) and Biopath (https://webapps.molecular-networks.com/biopath3/).
Database architecture and web interface
Integration of web tools/data access
Basic search and advanced search
The basic search is meant for users who are interested in the particular details of a carotenoid or a gene, pathway or organism. To further facilitate more precise searches and comparisons, the advanced search option has been provided. The option allows the user to fetch information for two carotenoids/genes/pathways/organisms at one time.
Tools available in the database
A tool for Structural search has been created which will be useful for the user interested in searching for carotenoids of similar or identical structure(s). We have also provided a BLAST tool for searching similar sequences in our database. Another tool for alignment and visualization has been created that will be useful for multiple sequence alignment. A self-explanatory help section was also created for providing basic information and knowhow for the database.
Utility and discussion
Cataloguing of information pertaining to carotenoids
In this category, the user can browse through different structural classes of the carotenoids along with their unique and total entries. Information on the following categories is provided: (i) Acyclic Carotenoids (with 40 unique entries and 721 total entries), (ii) Cyclic Carotenoids (with 31 unique entries and 359 total entries), (iii) Hydroxycarotenoids (with 75 unique entries and 479 total entries), (iv) Hydroxycarotenoids with cyclic structures (with 143 unique entries and 351 total entries), and (v) Unidentified carotenoids (with 15 unique entries and 29 total entries) (Fig. 2a and b). The user can obtain detailed information for each entry as a table containing information such as Molecular Weight, Molecular Formula, SMILES, IUPAC name, common name, InChI, InChIkey, chemical structures both in 2D and 3D format, UV Spectra, NMR spectra, HPLC data, etc. with their respective references.
Fifty different pathways involved in the synthesis of different structural categories of carotenoids can be browsed (Fig. 2c and d). The description of each pathway in the respective organism is provided in tabulated form, wherein information pertaining to the generalized pathway, corresponding genes, and carotenoids and organisms harboring that particular pathways are provided.
In ProCarDB, an option for browsing organisms for different categories of carotenoids is also available. This database suggests the presence of carotenoids across 611 organisms possessing carotenoids. Carotenoids have been identified and characterized in 304 organisms. Genome analyses revealed the presence of carotenoids in another 99 organisms. Remaining, 208 organisms are either pigmented or a preliminary study has suggested the presence of carotenoids while the detailed characterization of the carotenoid is yet to be performed (Fig. 2e).
This module is important for the taxonomist interested in analyzing the distribution of carotenoids across the prokaryotic kingdoms (Bacteria and Archaea) to the species level. This module will help them to reach a particular genera or species by following its hierarchy in the taxonomic classification. The number of carotenoids will be displayed at each taxonomic level.
The Genes category consists of 38 unique genes are distributed across the prokaryotes (Fig. 2f). These genes make up ~50 carotenoid biosynthesis pathways through various combinations and permutations and lead to synthesis of 304 unique carotenoids. Different genes responsible for the synthesis of different carotenoids are categorized for ease of browsing. Detailed information is also available in the form of a table containing information such as corresponding carotenoids, enzyme names, and organisms.
Applications of carotenoids
In this module, we have provided important notes on various applications of carotenoids. This webpage provides a link to important applications of carotenoids such as in prevention and protection from cancers, precursor of vitamin A, modulators of immune systems and as nutraceuticals. This section also describes the individual biological activity of each of the carotenoids.
Cataloguing and extension of pathways involved in the carotenoid biosynthesis
An example of extension of the pathways is the Astaxanthin pathway described in KEGG, that has been extended into a metabolic map that depicts the biosynthetic route for the formation of a number of derivatives of astaxanthin, such as 2-hydroxyastaxanthin and astaxanthin β-D glucoside . Another example of an extension of the metabolic pathway is the carotenoid erythroxanthin, which is synthesized in Brevundimonas sp. strain SD212; its pathway has been supported experimentally . However, the metabolic pathway(s) involved in the biosynthesis of erythroxanthin are not yet available in the KEGG map of carotenoid biosynthesis. Similarly, the Zeaxanthin pathway, the flavuxanthin pathway, and the bacterioruberin pathway have been studied in Cronobacter sakazakii , Corynebacterium glutamicum , and Halobacterium salinarium [45, 46], respectively. Although the zeaxanthin pathway is available in KEGG, there is no information for the flavuxanthin pathway or the bacterioruberin pathway. Hence, we believe that such extension of pathways involved in the carotenoid biosynthesis will be helpful to the researchers not only, to identify carotenoid intermediates but also to provide significant insights into predicting and characterizing the newer carotenoid biosynthesis pathways. These pathway-extensions make this database unique and one of the most updated information centres on the carotenoids. We have also predicted these pathways in every organism possessing carotenoids on the basis of validated or predicted pathways as published. These predictions have resulted in a tremendous increase in information and the information on pathways in each organism has been almost doubled, with approximately 33 % of pathways being predicted by us (Fig. 3b). Although these predictions need to be supported experimentally, they represent an important step forward and will tremendously help the researcher engaged in the elucidation of pathways of carotenoid synthesis.
Identification of organisms with potential for possessing carotenoids
ProCarDB is a comprehensive compilation of information pertaining to prokaryotic carotenoids. The major utility of this database is that it will help researchers’ worldwide working on carotenoids in the identification of carotenoids through its unique compilation of NMR data, UV data along with spectra, IR data, and HPLC data. This is an exclusive resource for researchers working on characterization of carotenoids. Additionally, this database assists users to find structurally similar carotenoids to their carotenoid of interest through a structure-based search tool and advance search tools. We have also provided the information about organisms and culture collections. Another important feature of this database is that it provides gene/enzyme sequences of components of pathways involved in the biosynthesis of prokaryotic carotenoids. It will be a great help for the cloning and expression of such genes in model organisms such as E. coli. This database is also equipped with a BLAST tool with which the users could investigate whether the genes/enzymes of interest might be involved in the biosynthesis of carotenoids. In summary, this database is a unique portal for information on carotenoids.
2D, 2 dimensional; 3D, 3 dimensional; BLAST, basic local alignment search tool; C20, 20 carbon unit; C5, five-carbon unit; CDB, conjugated double bonds; ChEBI, chemical entities of biological interest; CSS, cascading style sheets; HPLC, high-performance liquid chromatography; HTML, hypertext markup language; IJSEM, international journal of systematic and evolutionary microbiology; InChl, IUPAC international chemical identifier; IR, infrared; IUPAC, international union of pure and applied chemistry; KEGG, Kyoto encyclopedia of genes and genomes; LPSN, list of prokaryotic names with standing in nomenclature; MS, mass spectrometry; NMR, nuclear magnetic resonance; PHP, hypertext preprocessor (earlier called, personal home page); ProCarDB, prokaryotic carotenoid database; SMILES, simplified molecular-input line-entry system; UV, ultraviolet; UV-Vis, ultraviolet–visible
Nupur and Sandeep Kumar Dhanda are thankful to CSIR and ICMR, respectively, for senior research fellowships. Asheema Vats is thankful to CSIR for a fellowship and the Bioinformatics Center of the CSIR-Institute of Microbial Technology for its web services and the platform for ProCarDB. The authors are thankful to Dr. Shinichi Takaichi for reading the manuscript and suggestions regarding the database.
AKP is funded with OLP0075 from CSIR. The laboratory of AK is supported by DBT (BT/PR15097 and BT/PR15086/GBD/27/307/2011), DST (SR/SO/BB-0037/2013) and CSIR (OLP-70, BSC0119F, HCP0001, and BSC0211E) research grants.
Availability of data and materials
The database is freely available at bioinfo.imtech.res.in/servers/procardb. The database is system friendly with most of the operating system (including smart phone) but is best visualized in firfox/safari and is compatible with java 1.6.
The database was envisioned by Nupur, AV, AK, and AKP. The data was collected by Nupur. The database was designed by AV. The database was executed by AV, SKD and Nupur. The database was curated by AV, Nupur, SKD, GPSR, AK and AKP. MS was written by Nupur and AK. Editing of the manuscript was performed by AV, Nupur, SKD, GPSR, AK and AKP. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Ethics approval and consent to participate
Availability of supporting data
All the data associated with the manuscript can be downloaded from download section of the database with URL http://bioinfo.imtech.res.in/servers/procardb/?c=aboutus&m=downloads.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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