Subsystem: Carotenoid Biosynthesis
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1 Subsystem: Carotenoid Biosynthesis Olga Vassieva, Fellowship for Interpretation of Genomes Introduction Carotenoids are synthesised in plants, photosynthetic bacteria (carotenes, xanthins) and archaea (bacteriorhodopsin ) as components of light harvesting complexes and UV-protectors, as well as in nonphotosynthetic organisms - where their main function is UVprotection. Carotenoids differ by length of carbon skeleton (C-3,C-4, C-5 carotenoids), number and type of cyclic structures in a molecule (one or two rings of beta or epsilon conformation), presence of ketogroups, and types of carbohydrate side chains. About 3 genes involved in these pathways are currently known. Nevertheless, many steps of carotenoid biosynthesis are still a mystery, and genes encoding several enzymes of central importance have not been identified in a number of organisms, including cyanobacteria ( missing genes ).
2 Subsystem: Carotenoid biosynthesis (general list of known functions) Column Abbrev Functional Role 1 PS Phytoene synthase (EC ) 2 PDS Phytoene desaturase, pro-zeta-carotene producing (EC ) 3 NDS Neurosporene desaturase (EC ) 4 GPS Geranylgeranyl pyrophosphate synthetase (EC ) 5 CI Carotenoid cis-trans isomerase (EC ) 6 ZDS Pro-zeta-carotene desaturase, prolycopene producing (EC ) 7 Beta-carotene hydroxylase 8 Lycopene beta cyclase (EC ) 9 BCK Beta-carotene ketolase (EC ) 1 Lycopene epsilon cyclase 11 ZGT Zeaxanthin glucosyl transferase 12 PCS "phi-carotenoid synthase" (EC and EC ) 13 Hydroxyneurosporene synthase 14 HNM Hydroxyneurosporene methyltransferase (EC ) 15 PD Phytoene dehydrogenase and related proteins 16 VM CrtV-methyltransferase-like protein 17 TM CrtT-methyltransferase-like protein 18 F 2-vinyl bacteriochlorophillide hydratase (EC ) 19 PDSB Phytoene desaturase, neurosporene or lycopene producing (EC ) 2 DSS Dehydrosqualene synthase (EC ) 21 SD Squalene desaturase 22 SM Spheroidene/spirilloxanthin monooxygenase 23 LE Lycopene elongase 24 SRCB sigma-factor-like regulator of carotenoid biosynthesis 25 RCB Regulator of carotenoid biosynthesis
3 Organism Code PS PDS NDS GPS CI ZDS BCK ZGT PCS Synechocystis sp. PCC 683 [B] , Chlorobium tepidum TLS [B] Thermosynechococcus elongatus BP-1 [B] Synechococcus sp. WH 812 [B] marinus MED4 [B] marinus str. MIT 9313 [B] , marinus subsp. marinus str. CCMP1375 [B] Synechococcus elongatus PCC 7942 [B] Nostoc sp. PCC 712 [B] , Nostoc punctiforme [B] , , , Organism Code PS PDS NDS GPS CI ZDS BCK ZGT PCS Anabaena variabilis ATCC [B] Arabidopsis thaliana [E] , , 13592, 13594, 14243, 15259, 15387, 224, 21784, 21966, 4426, 741, 8858, 886, 12461, Crocosphaera watsonii WH 851 [B] , , , , Gloeobacter violaceus PCC 7421 [B] , , 394 Oryza sativa (japonica cultivargroup) [E] 5744 marinus subsp. pastoris str. CCMP1986 [B] Trichodesmium erythraeum IMS11 [B] Rhodobacter capsulatus SB13 [B] , 2896 Staphylococcus aureus NCTC 8325 [B] 1286 Organism Streptomyces avermitilis MA-468 [B] 125 Code PS PDS NDS GPS CI ZDS BCK ZGT PCS 124, , 1653, 2999, Subsystem: Carotenoid biosynthesis CYANOBACTERIA For notes and comments see subsystem (hyperlinked
4 Carotenoid biosynthesis Subsystem diagram FPP GPS I PS II PDS III ZDS IV DSS XXXI C-3 carotenoids, Staphylococcus Hypothetical reactions CYANOBACTERIA:MYXOXANTOPHYL BIOSYNTHESIS VI VII VIII IX ZGT ZDS X XI HNM NDS V XII C-4 carotenoids, Rhodobacter XXXII PDSB Retinal, Archaea ZDS ZDS PCS XXV XVI CI NDS Yellow pygments, Streptoyces PDSB XXIV XXIIII ZEAXANTINE XVII CI XIV GPS XV BCK XXVI XXVII CYANOBACTERIA :KETOCAROTENOID BIOSYNTHESIS XXI XIX LE SYNECHOCYSTIS NDS UTANTS XX Plant carotenoids XXVIII XXIX XXX PS P hytoene synthase (EC ), PDS1-Phytoene desaturase, pro-zeta-carotene producing NDS-Neurosporene desaturase,gps- -Geranylgeranyl pyrophosphate synthase (EC ) CI- Carotenoid cis-trans isomerase,zds- Pro-zeta-carotene desaturase, prolycopene producing,-- Beta-carotene hydroxylase (beta-carotene hydroxylase,,- Lycopene beta cyclase, BCK-Beta-carotene ketolase,--lycopene epsilon cyclase,zgt- -Zeaxanthin glucosyl transferase, P CS-"phi-Carotenoid synthase",- -Hydroxyneurosporene synthase HNM-Hydroxyneurosporene methyltransferase,p DSB-Phytoene desaturase, neurosporene or lycopene producing,dss- -Dehydrosqualene synthase,sd -Squalene desaturase, SM- - Spheroidene/spirilloxanthin monooxygenase LE- -Lycopene elongase C-5 carotenoids, Corynobacterium, Archaea I-Farnesyl pyrophosphate I-Geranylgeranyl pyrophosphate II- P hytoene III-all-trans zeta-carotene IV-trans-Lycopene V- neurosporene VI-3,4- didehydroneurosporene VII-3,4-didehydrolycopen VIII-torulene IX-deoxymyxol X-Deoxymyxol 2'-(2,4-di-O methyl-alpha-l-fucoside XI-Deoxymyxol 2'-(2,4-dimethyl-alpha-L-fucoside XII-ihydroxyneurosporene XIII-trans Lycopene XIV-Zeaxantine XV-beta-Carotene XVIcis zeta-carotene XVIIIcis Lycopene XIXgamma-Carotene XXalpha-Carotene XXIdelta-Carotene XXIIlutein XXIII-astaxanthin XXIV-canthaxanthin XXV-beta-isorenieratene XXVI-Echinenone XXVII-3'-Hydroxyechinen XXVIII-3,4- dihydrodeoxymyxol XXIX-3,4-dihydromyxol XXX-3,4-dihydromyxol mo o di-methylfucoside XXXI-diapophytoene XXXII-retinal
5 Subsystem diagram FPP GPS I PS II PDS III ZDS IV DSS XXXI C-3 carotenoids, Staphylococcus In Synechocystis N. punctiforme Trichodesmium SYNECHOCYSTIS:MYXOXANTOPHYL BIOSYNTHESIS VI VII VIII IX ZGT ZDS X XI HNM NDS V XII PDSB ZDS ZDS C-4 carotenoids, Rhodobacter PDSB PCS XXV XVI CI NDS Yellow pygments, Streptoyces XXIV XXIIII Functions present in all cyanobacteria Absent in all cyanobacteria only in Nostoc sp. ZEAXANTINE XVII CI XIV GPS XV BCK XXVI XXVII BCK XXI XIX -absent in S. elongatus, T. elongatus only in plants, Prochlorococci, Synechococcus WH 812 CYANOBACTERIA :KETOCAROTENOID BIOSYNTHESIS is missing from Synechocystis 683, Nostoc sp, A.variabilis, Crocosphaera LE SYNECHOCYSTIS NDS UTANTS XX Plant carotenoids XXVIII XXIX XXX C-5 carotenoids, Corynobacterium, Atchaea
6 Open questions, comments, conjectures. 1. The case of missing beta-carotene ketolase Organism PS PDS NDS GPS CI ZDS BCK Code Synechocystis sp. XV PCC 683 [B] , Chlorobium tepidum TLS [B] 1367 BCK Thermosynechococc us elongatus BP-1 XXVI [B] Synechococcus sp. WH 812 [B] marinus MED4 [B] marinus str. MIT Echinenone astaxanthin -canthaxanthin CYANOBACTERIA :KETOCAROTENOID BIOSYNTHESIS 9313 [B] , marinus subsp. marinus str. CCMP1375 [B] Synechococcus elongatus PCC 7942 [B] Nostoc sp. PCC 712 [B] , Nostoc punctiforme [B] , , , 772 Biosynthesis of keto-carotenoids depends on beta- Anabaena variabilis ATCC [B] , Crocosphaera watsonii WH 851 [B] , carotene ketolase 13594, known in bacteria as the product of crtw or crto genes 4853, , , crto Our annotation Our annotati 3% homolo to carotene isomerase Our annotation: 3% homology to fatty acid desaturases (characteristic for plant carotene ketolases/hydroxylases). Circadian clock cluster. Homologs in all Prochlorococci crto crto crto
7 Open questions, comments, conjectures. 2. The case of missing glycosyl transferase Synechocystis sp. PCC 683 [B] , Chlorobium tepidum TLS [B] Thermosynechococcus elongatus ZDS BP-1 [B] Synechococcus sp. WH 812 [B] marinus MED4 [B] marinus str. MIT 9313 [B] , marinus subsp. marinus str. CCMP1375 [B] 166 VIII Synechococcus elongatus PCC 7942 [B] Nostoc sp. PCC 712 [B] , Nostoc punctiforme [B] , , , Organism Organism Arabidopsis thaliana [E] Code PS PDS NDS GPS CI ZDS BCK ZGT Code PS PDS NDS GPS CI ZDS BCK ZGT 3,4-didehydro neurosporene CYANOBACTERIA:MYXOXANTOPHYL BIOSYNTHESIS VII IX 4853, Anabaena variabilis ATCC [B] ZGT , 2233, 138, HNM 13592, Crocosphaera watsonii WH 851 [B] involves crtx 4133 gene product , 14243, X Deoxymyxol 2 -(2,4-di-O-methylalpha-L-fucoside 19124, , 15387, 224, 21784, 21966, 4426, 741, 8858, Biosynthesis of UV-protective carotenoid myxoxanthophyll Zeaxanthin glycosyl transferase. Most of other enzymes of the proposed pathway in cyanobacteria are still unknown 886, 12461, , cr 25% homology crtx
8 Case 3. The case of missing beta-lycopene cyclase Organism Code PS PDS NDS GPS CI ZDS BCK Synechocystis sp. PCC 683 [B] , Chlorobium tepidum TLS [B] Thermosynechococc us elongatus BP-1 [B] Synechococcus sp. WH 812 [B] marinus MED4 [B] marinus str. MIT 9313 [B] , marinus subsp. marinus str. CCMP1375 [B] Synechococcus elongatus PCC 7942 [B] Nostoc sp. PCC 295, 712 [B] Nostoc punctiforme [B] , , , 772 Anabaena variabilis 4853, ATCC [B] , Crocosphaera 13592, 138, watsonii WH 851 [B] , 14243, 2233, %homolo
9 Search for gene candidates for the role of missing lycopene cyclase Gene candidates were selected on the basis of (i) functional clustering with known genes of carotenoid biosynthesis pathway (7 candidates), and/or (ii) sequence similarity with known forms of lycopene cyclase (6 candidates). Hypothetical proteins as well as hypothetical cyclases, synthases, and dehydrogenases were considered. Since known lycopene cyclases are membrane proteins, hypothetical proteins with predicted transmembrane domains were preferentially selected. Occurrence profile was used as an additional filter: gene candidates were ranked based on the presence of their clear homologs in all genomes lacking known lycopene cyclase (several cyanobacteria and Chlorobium tepidum - see previous slide) and their absence from the genomes where lycopene cyclase homolog(s) have been identified (e.g. Synechococcus sp. WH 812 and Prochlorococci).
10 Gene candidates for the role of missing lycopene cyclase identified in cyanobacter I: Oligoketide cyclase/lipid transport protein homolog (example: Slr941 in Synechocystis 683) Supporting evidences: (i) homologous to oligoketide cyclase/lipid transport protein, (ii) is a membrane protein, (iii) very strong chromosomal clustering: is co-localized with orthologs of pro-zeta-carotene desaturase, prolycopene producing (ZDS) in nearly all analyzed cyanobacterial genomes. Negative features: (i) orthologs are present in Prochlorococci, and (ii) absent in the genome of Chlorobium tepidum. II: Two closely related hypothetical dehydrogenases (examples: Sll659 and Sll147) Supporting evidences: (i) nearly perfect occurrence profile, (ii) proposed function dehydrogenase, (iii) presence a UbiH domain (Ubiquinone biosynthesis reductase), hence potential activity towards related isoprenoid derivatives, (iv) distant homology with lycopene cyclase (CrtL) from Prochlorococci. III: Putative farnesyl diphosphate farnesyl transferase (example: Sll513 in Synechocystis 683) Supporting evidences: (i) highly homologous to phytoene/squalene synthetase and/or farnesyl diphosphate farnesyltransferase (EC ), (ii) distant homology to lycopene cyclase / phytoene synthase from Blakeslea trispora, (iii) satisfactory occurrence profile, (iv) is a membrane protein. Negative feature: absent in the genomes of Chlorobium tepidum and T. elongates IV: Hypothetical protein (example: Slr1579 in Synechocystis 683) Supporting evidence: (i) homology, albeit distant, with CrtYm (monocyclic)-lycopene cyclase, functionally analogous to the one inferred in Synechocystis 683 (monocyclic lycopene cyclase). This low homology may be still meaningful, since CrtYm has the same low homology to Prochlorococci lycopene cyclase (CrtY). Negative feature: absent in Chlorobium tepidum V: Hypothetical protein (example: Slr1394 in Synechocystis 683) Supporting evidence: (i) strong chromosomal clustering with geranylgeranyl pyrophosphate synthase (GPS) in cyanobacteria (excluding Synechocystis 683), (ii) integral membrane protein, (iii) orthologs are evident in plants, (iv) satisfactory occurrence. Negative features: ortholog is absent in Chlorobium tepidum, and present (rather distant however) in Prochlorococci and Synechococcus sp. WH 812. Cyclase or carotene p45 oxygenase/hydroxylase Supporting evidence: (i) chromosomal coupling with beta-caroten ketolase (EC ). Distant homolog of lycopene cyclase/phytoene synthase from Blakeslea trispora
11 Gene candidates for missing functional roles in carotenoid biosynthesis: occurrence profile in cyanobacterial genomes. Organism/prote in I II III IV V p45 Synechocystis sp. PCC 683 Chlorobium tepidum TLS Thermosynechoc occus elongatus BP-1 Synechococcus sp. WH 812 marinus MED4 marinus str. MIT 9313 marinus subsp. marinus str. CCMP1375 Synechococcus elongatus PCC 7942 slr941 sll659/ sll147 gi sll513 slr1579 slr1394 slr574 gi , /gi gi gi gi gi gi gi gi <25% homology gi gi gi (only 18% homology) gi <5% homology gi gi gi gi gi gi Nostoc sp. PCC 712 gi gi / gi gi gi gi gi Nostoc punctiforme gi gi / gi gi gi gi gi Anabaena variabilis ATCC gi Alr185 protein gi gi gi 1534 Crocosphaera w, WH851 Trihodesmium IMS11 ref ZP_ gi / gi gi gi gi gi gi gi gi gi gi gi
12 Case 4. Predicted carotenoid glycosyl transferase Synechocystis sp. PCC 683 [B] Chlorobium tepidum TLS [B] Thermosynechococc us elongatus BP-1 [B] Synechococcus sp. WH 812 [B] marinus MED4 [B] marinus str. MIT 9313 [B] marinus subsp. marinus str. CCMP1375 [B] Synechococcus elongatus PCC 7942 [B] Nostoc sp. PCC 712 [B] Homologs present in the all cyanobacterial genomes Example: gi (SYNW729) in Synechococcus sp. WH 812 Current annotation in this organism: Glycosyltransferase (EC ) Clustering with lycopene cyclase in Synechococcus sp. WH 812 and Prochlorococci Annotations in other organisms: hypothetical protein Nostoc punctiforme [B] Anabaena variabilis ATCC [B] Crocosphaera w, WH851 Trihodesmium IMS11
13 Case 5. Strong functional coupling of hypothetical ORFs with known genes of isoprenoid or carotenoid biosynthesis may be indicative of their potential role in these pathways Crocosphaera watsonii WH Synechococcus sp.wh 812 Nostoc punctiforme marinus Synechococcus sp.wh Genes related to isoprenoid/carotenoid biosynthesis (open arrows): 1: Carotene isomerase 2: Phytoene desaturase, z-carotene producing 3: 1-deoxy-D-xylulose-5-P reductoisomerase 4: Ubiquinone monoxygenase UbiB Gene candidates (solid arrows), annotated currently as: 5: hypothetical P-loop- ATPasenucleotidyltransfrase 6: motif: prenyl binding site 7: Olidoketide cyclase/lipid transport protein 8: sensory transduction histidine kinase Synechococcus elongatus Pyrococcus horikoshii Aquifex aeolicus VF
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