Comprehensive Analyses of Cytochrome P450 Monooxygenases and Secondary Metabolite Biosynthetic Gene Clusters in Cyanobacteria
Abstract
:1. Introduction
2. Results and Discussion
2.1. Cyanobacterial Species Have Lowest Number of P450s
2.2. CYP110 is the Dominant P450 Family in Cyanobacterial Species
2.3. Cyanobacterial Species Have Lowest Secondary Metabolite Biosynthetic Gene Clusters
2.4. Cyanobacterial Species Has Highest Gene Cluster Diversity Percentage Compared to Bacillus and Mycobacterial Species
2.5. Few Cyanobacterial Species P450s Found to be Part of Secondary Metabolite Biosynthetic Gene Clusters
2.6. Cyanobacterial Species P450s Functions and Features Resemblance to Eukaryotic P450s
3. Materials and Methods
3.1. Species and Databases
3.2. Genome Data Mining and Annotation of P450s
3.3. Phylogenetic Tree Construction of Cyanobacterial Species P450s
3.4. Generation of P450 Profile Heat-Maps
3.5. Secondary Metabolite Biosynthetic Gene Clusters Analysis
3.6. Data Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Species Name | Well Known for | Reference(s) |
---|---|---|
Acaryochloris marina | Species were isolated from the marine environment and can produce chlorophyll d as primary photosynthetic pigment that is able to use far-red light for photosynthesis. | [18] |
Anabaena sp. WA102 | Filamentous nitrogen-fixing cyanobacterium that often form blooms in eutrophic water bodies and able to produce a range of neurotoxic secondary metabolites. | [19] |
Synechocystis sp. PCC 6803 | Species found in fresh water and capable of both phototrophic and heterotrophic growth; owing to this ability, it was one of the most highly studied cyanobacterium for these characteristics. This species lost its nitrogen-fixing ability. | [20] |
Synechococcus elongatus PCC 6301 | Unicellular, rod-shaped, fresh-water living, obligate photoautotrophic organism that has long been used as a model organism for photosynthesis research. | [21] |
Synechococcus sp. WH8102 | Widely found in marine water across the world. It is well known for its oligotrophic nature, as it can utilize nitrogen and phosphorus sources. It also developed strategies to conserve limited iron stores by using nickel and cobalt in some enzymes. Species belonging to the genus Synchococcus are considered generalist compared to Prochlorococcus species, as they are nutritionally versatile and adapted to different ecological niches. These species developed a unique type of swimming motility, as they propel in the absence of any demonstrable external organelle. | [22] |
Thermosynechococcus elongates | This species is unique among cyanobacterial species, as it grows in hot springs and has an optimal growth temperature of 55 °C. | [23] |
Cyanobium sp. NIES-981 | This species is used for standard inhibition tests for toxicants in water, as it fulfills the criteria provided by the Organization for Economic Co-operation and Development test guidelines. | [24] |
Dactylococcopsis salina | Gas-vacuolate cyanobacterium isolated from Solar Lake, a stratified heliothermal saline pool in Sinai. | [25] |
Chamaesiphon minutus | It is an epiphyte of fresh water red alga Paralemanea catenata (Rhodophyta). | [26] |
Leptolyngbya sp. NIES-3755 | Species belonging to this genus are found in various environments ranging from soil and fresh water to hypogean sites. This species was isolated from the soil at the Toyohashi University of Technology, Japan. | [27,28,29] |
Halomicronema hongdechloris | It is the first cyanobacterium to be identified that produces chlorophyll f and is isolated from a stromatolite in the World Heritage site of Shark Bay, Western Australia. | [30,31] |
Pseudanabaena sp. ABRG5-3 | It is a semifilamentous, non-heterocystous cyanobacterium isolated from a pond in Japan. | [32] |
Prochlorococcus marinus subsp. marinus CCMP1375 | Among species of the Prochlorococcus genus, this cyanobacterium is extreme as it can grow at very low light levels in the ocean. Species belonging to this genus are the smallest known oxygen-evolving autotrophs and dominate the tropical and subtropical oceanic phytoplankton community. Species in this genus are adapted to different light levels in the ocean. | [33] |
Geminocystis sp. NIES-3709 | Fresh water living cyanobacterium capable of accumulating large amounts of phycoerythrin, light-harvesting antenna proteins, compared to Geminocystis sp. NIES-3708. | [34] |
Microcystis aeruginosa | Species belonging to this genus are the most representative of toxic bloom-forming cyanobacteria in eutrophic waters. M. aeruginosa is well-known for its toxicity by producing various toxic small polypeptides, including microcystin and cyanopeptolin. | [35] |
Cyanobacterium sp. Strain HL-69 | It is isolated from the magnesium sulfate-dominated hypersaline Hot Lake in northern Washington. | [36] |
Crocosphaera watsonii | Nitrogen-fixing cyanobacterium found in oligotrophic oceans adapted to iron and phosphorus limitation. | [37] |
Crocosphaera subtropica | Unicellular cyanobacteria capable of fixing atmospheric dinitrogen (diazotroph) in marine environments, like filamentous cyanobacterial species. | [38] |
Trichodesmium erythraeum | Filamentous cyanobacterium known as the primary producer and supplier of new nitrogen through its ability to fix atmospheric dinitrogen (diazotroph) in tropical and subtropical oceans. | [39] |
Arthrospira (Spirulina) platensis | Economically important cyanobacterium, an important source of nutrition and medicinal value. This species is consumed as a source of protein around the world. | [40] |
Planktothrix agardhii | Cyanobacterium forming bloom in eutrophic water and capable of producing toxins. | [41] |
Moorea producens | Prolific secondary metabolite producing filamentous tropical marine cyanobacterium. One-fifth of its genome is devoted to the production of secondary metabolites. | [42] |
Gloeobacter violaceus | Ancient cyanobacterium that lacks thylakoid membranes. | [43] |
Nostoc sp. PCC 7120 | Filamentous cyanobacterium capable of fixing atmospheric dinitrogen (diazotroph). | [44] |
Nostoc punctiforme | A facultative heterotroph symbiotic cyanobacterium capable of establishing symbiosis with Anthoceros punctatus. | [45] |
Nostoc azollae 0708 | A nitrogen-fixing endosymbiont of water fern Azolla filiculoides Lam. | [46] |
Anabaena sp. strain 90 | Hepatotoxic bloom-forming cyanobacterium with 5% of its genome devoted to synthesis of small peptides that are toxic to animals. | [47] |
Calothrix strain 336/3 | Industrially relevant cyanobacterium capable of producing higher levels of hydrogen (biofuel) compared to N. punctiforme PCC 73102 and Nostoc (Anabaena) sp. strain PCC 7120. | [48] |
Fischerella sp. NIES-3754 | Cyanobacterium isolated from hot spring in Japan with potential to have thermoresistant optogenetic tools. | [49] |
Nodularia spumigena UHCC 0039 | Cyanobacterium responsible for Baltic sea brackish water cyanobacterial blooms producing toxins. | [50] |
Cyanobacterial Species | Bacillus Species | Mycobacterial Species | Streptomyces Species | |
---|---|---|---|---|
Total No. of Species Analyzed | 114 | 128 | 60 | 48 |
No. of P450s | 341 | 507 | 1784 | 1625 |
No. of Families | 36 | 13 | 77 | 144 |
No. of Subfamilies | 79 | 28 | 132 | 377 |
Dominant P450 family | CYP110 | CYP107 | CYP125 | CYP107 |
No. of BGCs * | 770 | 1098 | 898 | 1461 |
Types of BGCs | 73 | 33 | 18 | 159 |
No. of P450s Part of BGCs | 27 | 112 | 204 | 554 |
Average No. of P450s | 3 | 4 | 30 | 34 |
P450 Diversity Percentage | 0.09 | 0.02 | 0.07 | 0.18 |
Average No. of BGCs | 7 | 9 | 15 | 30 |
Gene Cluster Diversity Percentage | 0.08 | 0.02 | 0.03 | 0.23 |
Percentage of P450s Part of BGCs | 8 | 22 | 11 | 34 |
Reference | This work | [54] | [55,59] | [55] |
P450 Names | Type of Clusters | Most Similar Known Cluster | Similarity |
---|---|---|---|
CYP213A8 | T3PKS | Xenocyloins | 25% |
CYP213A5 | bacteriocin | ||
CYP213A6 | T3PKS | Colicin V | 2% |
CYP110AH1 | NRPS | Anabaenopeptin NZ 857/nostamide A | 100% |
CYP213A3 | bacteriocin | ||
CYP120C2 | T2PKS | Ambiguine | 6% |
CYP110K6 | NRPS | ||
CYP120A21 | bacteriocin | ||
CYP110Q3 | NRPS, T1PKS | Hapalosin | 40% |
CYP110C17 | terpene | ||
CYP110C29 | NRPS, T1PKS | Nostophycin | 27% |
CYP1011G1 | NRPS, T1PKS | Crocacin | 23% |
CYP110AP1 | terpene | ||
CYP110AT1 | NRPS, T1PKS | Hapalosin | 40% |
CYP110Q4 | NRPS, T1PKS | Hapalosin | 40% |
CYP110C21 | NRPS-like | Anacyclamide | 14% |
CYP197E3 | NRPS, T1PKS | Cryptophycin | 37% |
CYP110AG1 | terpene | Hectochlorin | 25% |
CYP110E29 | terpene, thiopeptide, T1PKS, NRPS | Nostophycin | 27% |
CYP110E18 | terpene, thiopeptide, T1PKS, NRPS | Nostophycin | 27% |
CYP110C21 | terpene | ||
CYP110Q4 | NRPS, T1PKS | Puwainaphycins | 40% |
CYP110AT1 | NRPS, T1PKS | Puwainaphycins | 40% |
CYP120A13 | ladderane | ||
CYP1185A1 | lassopeptide, bacteriocin | ||
CYP110Q2 | NRPS, T1PKS | Hapalosin | 40% |
CYP110C14 | terpene | 6,6′-oxybis(2,4-dibromophenol) | 14% |
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Khumalo, M.J.; Nzuza, N.; Padayachee, T.; Chen, W.; Yu, J.-H.; Nelson, D.R.; Syed, K. Comprehensive Analyses of Cytochrome P450 Monooxygenases and Secondary Metabolite Biosynthetic Gene Clusters in Cyanobacteria. Int. J. Mol. Sci. 2020, 21, 656. https://doi.org/10.3390/ijms21020656
Khumalo MJ, Nzuza N, Padayachee T, Chen W, Yu J-H, Nelson DR, Syed K. Comprehensive Analyses of Cytochrome P450 Monooxygenases and Secondary Metabolite Biosynthetic Gene Clusters in Cyanobacteria. International Journal of Molecular Sciences. 2020; 21(2):656. https://doi.org/10.3390/ijms21020656
Chicago/Turabian StyleKhumalo, Makhosazana Jabulile, Nomfundo Nzuza, Tiara Padayachee, Wanping Chen, Jae-Hyuk Yu, David R. Nelson, and Khajamohiddin Syed. 2020. "Comprehensive Analyses of Cytochrome P450 Monooxygenases and Secondary Metabolite Biosynthetic Gene Clusters in Cyanobacteria" International Journal of Molecular Sciences 21, no. 2: 656. https://doi.org/10.3390/ijms21020656