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132,173-Cyclopheophorbide B Enol As a Catabolite of Chlorophyll B In View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector FEBS Letters 587 (2013) 2578–2583 journal homepage: www.FEBSLetters.org 132,173-Cyclopheophorbide b enol as a catabolite of chlorophyll b in phycophagy by protists ⇑ Yuichiro Kashiyama a,b,c, , Akiko Yokoyama d, Takashi Shiratori d, Isao Inouye d, Yusuke Kinoshita a, ⇑ Tadashi Mizoguchi a, Hitoshi Tamiaki a, a Graduate School of Life Sciences, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan b Department of Environmental and Biological Chemistry, Fukui University of Technology, Fukui, Fukui 910-8505, Japan c Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency (JST), Chiyoda, Tokyo 153-8902, Japan d Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan article info abstract Article history: Both 132,173-cyclopheophorbide a and b enols were produced along with ingestion of green Received 9 May 2013 microalgae containing chlorophylls a and b by a centrohelid protist (phycophagy). The results sug- Revised 24 June 2013 gest that chlorophyll b as well as chlorophyll a were directly degraded to colored yet non-phototoxic Accepted 25 June 2013 catabolites in the protistan phycophagic process. Such a simple process by the predators makes a Available online 4 July 2013 contrast to the much sophisticated chlorophyll degradation process of land plants and some algae, where phototoxicity of chlorophylls was cancelled through the multiple enzymatic steps resulting in Edited by Richard Cogdell colorless and non-phototoxic catabolites. Ó 2013 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved. Keywords: Aquatic ecosystem Chlorophyll catabolism Cyclopheophorbide enol Microalga Phycophagy Protist 1. Introduction colorless, non-fluorescent catabolites, hence abolishing the photo- toxicity of Chls in the plant tissues. Chlorophylls (Chls) are essential components of the photosyn- Recently, a second degradation process of Chl-a (4) has been thetic apparatus, and thus significant molecules for living organ- proposed [2], which is conducted in cells of phycophagic protists isms and environments. Whereas the biosynthesis of Chls is (protists feeding on microalgae) following their ingestion of algal relatively well understood, studies on their biodegradative pro- diets. The resulting product was 132,173-cyclopheophorbide a enol cesses are still limited. In land plants, Chl-a (4 in Fig. 1) is decom- (cPPB-aE; 11), which is a green colored but non-fluorescent pig- posed step-by-step, where pheophorbide a oxygenase (PAO) plays ment. Due to its non-phototoxicity, cPPB-aE represents another a central role that cleaves the tetrapyrrole macrocycle generating a detoxified catabolite of Chl-a. The catabolite is ubiquitously de- linear tetrapyrrolic catabolite, a so-called PAO-pathway [1]. The tected in oceans and lakes where large amounts of cPPB-aE are catabolism through the PAO-pathway eventually results in accumulated as the most abundant Chl-a-derived degradation product [2,3]. Therefore, cPPB-aE metabolism is a widely distrib- uted degradation process of Chl-a in aquatic ecosystems. Abbreviations: APCI, atmospheric pressure chemical ionization; Chl, chlorophyll; Little has been understood about the degradation of other Chl cPPB-aE, 132,173-cyclopheophorbide a enol; cPPB-bE, 132,173-cyclopheophorbide b molecules along with protistan phycophagy, including Chl-b (1) enol; PAO, pheophorbide a oxygenase; PDA, photodiode array; Phe, pheophytin; in green algae. Green algae include diverse forms of aquatic micro- PPB, pheophorbide; pPhe, pyropheophytin; pPPB, pyropheophorbide; (R/S)-hCPLs, and macroalgae as well as land plants (embryophytes) and com- (132R)- and (132S)-hydroxychlorophyllones; TOF, time-of-flight monly produce Chl-b as an accessory pigment in photosynthetic ⇑ Corresponding authors at: Graduate School of Life Sciences, Ritsumeikan University, Kusatsu, Shiga 525-8577, Japan. Fax: +81 776297891 (Y. Kashiyama), antenna. Chl-b in land plants is known to be decomposed through +81 775612659 (H. Tamiaki). the PAO-pathway, where Chl-b is first converted into Chl-a in a E-mail addresses: [email protected] (Y. Kashiyama), [email protected] two-step enzymatic process, and further decomposed [1]. Such a (H. Tamiaki). 0014-5793/$36.00 Ó 2013 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.febslet.2013.06.036 Y. Kashiyama et al. / FEBS Letters 587 (2013) 2578–2583 2579 O R1 N N Chl-b (1): M = Mg; R = COOMe N N Chl-a (4): M = Mg; R = COOMe NH N M Phe-b (2): M = 2H; R = COOMe M Phe-a (5): M = 2H; R = COOMe N N pPhe-b (3): M = 2H; R = H N N pPhe-a (6): M = 2H; R = H N HN R O R O O O a 7 1 2 O O O O OR2 pPPB- ( ): R = Me; R = H pPPB-b (8): R1 = CHO; R2 = H Methyl pPPB-b (9): R1 = CHO; R2 = Me O O O NH N NH N NH N NH N NH N N HN N HN N HN N HN N HN OH OH O H O OH O OH O O O O O cPPB-bE (10) cPPB-aE (11) Diketone form of 10 (12) (R/S)-hCPL-b (13) (R/S)-hCPL-a (14) Fig. 1. Chemical structures of natural chlorophylls (Chls) and their derivatives. controlled degradation of the phototoxic Chl-b is expected also in 2.2. Feeding experiments aquatic ecosystems, because green ‘‘plants’’ are important compo- nents particularly in fresh water environments (i.e., microalgae Feeding experiments were designed for the above maintained including such familiar genera as Chlamydomonas, Chlorella, Closte- centrohelid SRT127, to which an aliquot of unialgal culture of Pyra- rium, Pediastrum, Spyrogyra, Staurastrum, and Volvox). For example, mimonas sp. (DA140) was added periodically every 3 to 10 days. a green alga Chlorella protothecoides was reported to conduct a The mixture was incubated at 20 °C in artificial seawater (Wako) PAO-like chlorophyll degradation, where both Chl-a and Chl-b enriched with Daigo’s IMK medium under RGB LED light at were directly converted into linear-tetrapyrrolic catabolites [4]. 16 lmol photon mÀ2 sÀ1, and the whole culture were filtrated We here report quantitatively significant occurrences of a Chl-b through sterile GF/F filters (Whatman, 47 mm /; GE Healthcare, derivative that is analogous to cPPB-aE, along with the consump- Buckinghamshire, UK). Total incubation periods were typically tion of green microalgae by phycophagic protists, hence proposing 20 days. Cultured cells of SRT127 were isolated from the above a direct degradation pathway of Chl-b (1)to132,173-cyclopheo- mixture containing DA140 by micropipetting, co-cultured with phorbide b enol (cPPB-bE; 10), without conversion to Chl-a in the cryptomonad (OR1), then incubated at 20 °C in filtration-ster- advance. ilized natural seawater enriched with an ESM medium for 5 days before filtration through GF/F filters. The GF/F filters were immedi- 2. Materials and methods ately frozen and stored in À20 °C before pigment extraction. 2.1. Strains of protists 2.3. Sample preparation A strain of a colorless centrohelid (SRT127; undescribed) was Each wet filter was extracted three times by ultrasonication in isolated by micropipetting from a seawater sample collected at a acetone (‘‘dioxin analysis’’ grade; Wako Pure Chemicals) for wharf of Tokyo Bay, Tokyo, Japan (35° 370 500 N, 139° 460 2300 W) 5 min at 0 °C in the dark. An aliquot of ethanol (‘‘dioxin analysis’’ on July 30, 2011. SRT127 was co-cultured with a strain of green grade, Wako Pure Chemicals) was added to the combined extracts, alga, Pyramimonas sp. (DA140), which was also isolated from the then dried in vacuo in the dark. The residue was dissolved in ani- Ò same location. Unialgal DA140 cultures as well as co-cultures of sole (‘‘RegentPlus ’’ grade; Sigma–Aldrich, St. Louis, USA) just be- SRT127 with DA140 were maintained at 18 °C in filtration- fore analysis. All of the above operations were performed under sterilized natural seawater enriched with Daigo’s IMK medium argon atmosphere using a glove box. for marine microalgae (Wako Pure Chemicals, Osaka, Japan) under fluorescent lights at 12 lmol photon mÀ2 sÀ1. A strain of a crypto- 2.4. HPLC analysis/isolation of pigments monad alga Chroomonas sp. (OR1) was isolated by micropipetting from a seawater sample collected at Ooarai Sun Beach, Ooarai Iba- Analytical HPLC was performed using a Shimadzu Prominence raki, Japan (36° 180 1000 N, 140° 340 500 W) on June 23, 2010, which liquid chromatograph system, comprised of a CBM-20A communi- was maintained at 18 °C in filtration-sterilized natural seawater cations bus module, a DGU-20A5R degasser, three LC-20AD pumps enriched with an ESM medium [5] under fluorescent lights (Cool constituting a ternary pumping system, an SIL-20AC auto sampler, White Fluorescent Lamp; Mitsubishi OSRAM, Yokohama, Japan) a CTO-20AC column oven, an SPD-M20Avp photodiode array (PDA) at 12 lmol photon mÀ2 sÀ1. detector, and an FRC-10 automated fraction collector (Kyoto, 2580 Y. Kashiyama et al. / FEBS Letters 587 (2013) 2578–2583 (R)-hCPL-a (13) (S)-hCPL-a (13) cPPB-aE (11) Chl-a (4) Phe-b (2) Phe-a (5) pPhe-a (6) b 1 a’ b 3 A pPPB-b (8) pPPB-a (7) Chl- ( ) Chl- pPhe- ( ) 400 500 600 700 5 10 15 20 25 B cPPB-bE (10) 400 500 600 700 C 5 10 15 20 25 400 500 600 700 5 10 15 20 25 x y z (carotenoid) Chl-b’ D 400 Wavelength (nm) 500 600 700 5 10 15 20 25 Fraction I Fraction II E 400 500 600 700 5 10 15 20 25 F 400 500 600 700 5 10 15 20 25 Retention time (min) Fig.
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