Extracellular Vesicle-Mediated Secretion of Chlorophyll Biosynthetic Intermediates in the Cyanobacterium Leptolyngbya Boryana

Overview

Journal Plant Cell Physiol

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2024 Aug 22

PMID 39172638

Authors

Kentaro Usui

Haruki Yamamoto

Hitoshi Mori

Yuichi Fujita

Affiliations

Soon will be listed here.

Abstract

Extracellular vesicles (EVs) are derived from outer membranes (OMs) in Gram-negative bacteria and have diverse physiological functions. EV-mediated secretion of monovinyl protochlorophyllide (MV-Pchlide), the chlorophyll a (Chl) biosynthetic intermediate, was previously reported in a mutant lacking dark-operative Pchlide reductase in the cyanobacterium Leptolyngbya boryana. This study showed a detailed characterization of EVs from wild-type (WT) strain of L. boryana grown under photoautotrophic and dark heterotrophic conditions, focusing on the accumulation of Chl intermediates. WT L. boryana cells produce two types of EVs, low-density EVs (L-EVs) and high-density EVs (H-EVs), both under light and dark conditions. L-EVs and H-EVs showed distinct morphological features and protein compositions. L-EVs from cells grown under both light and dark conditions commonly contained carotenoids, ketomyxol glycoside and zeaxanthin as major pigments. Based on the protein compositions of EVs and other cellular membrane fractions, L-EVs and H-EVs are probably derived from low-density OMs and high-density OMs interacting with cell walls, respectively. Fluorescence detection of pigments was applied to EVs, and the two Chl intermediates, protoporphyrin IX and protoporphyrin IX monomethyl ester, were commonly detected in both L-EVs from light- and dark-grown cells, whereas L-EVs from dark-grown cells contained additional MV-Pchlide, MV-protopheophorbide and pheophorbide. The pigment ratios of L-EVs to the total culture medium of the Chl intermediates were much higher than those of carotenoids, suggesting an active transport of the Chl intermediates from the thylakoid membrane to L-EVs. Cyanobacterial EVs may play a novel role in alleviating the accumulation of Chl intermediates in cells.

References

Fujita Y, Takagi H, Hase T . Cloning of the gene encoding a protochlorophyllide reductase: the physiological significance of the co-existence of light-dependent and -independent protochlorophyllide reduction systems in the cyanobacterium Plectonema boryanum. Plant Cell Physiol. 1998; 39(2):177-85. DOI: 10.1093/oxfordjournals.pcp.a029355. View

Tanaka R, Tanaka A . Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol. 2007; 58:321-46. DOI: 10.1146/annurev.arplant.57.032905.105448. View

Yamanashi K, Minamizaki K, Fujita Y . Identification of the chlE gene encoding oxygen-independent Mg-protoporphyrin IX monomethyl ester cyclase in cyanobacteria. Biochem Biophys Res Commun. 2015; 463(4):1328-33. DOI: 10.1016/j.bbrc.2015.06.124. View

Obata D, Takabayashi A, Tanaka R, Tanaka A, Ito H . Horizontal Transfer of Promiscuous Activity from Nonphotosynthetic Bacteria Contributed to Evolution of Chlorophyll Degradation Pathway. Mol Biol Evol. 2019; 36(12):2830-2841. DOI: 10.1093/molbev/msz193. View

Duperthuy M, Sjostrom A, Sabharwal D, Damghani F, Uhlin B, Nyunt Wai S . Role of the Vibrio cholerae matrix protein Bap1 in cross-resistance to antimicrobial peptides. PLoS Pathog. 2013; 9(10):e1003620. PMC: 3789753. DOI: 10.1371/journal.ppat.1003620. View

Biller S, Del Carmen Munoz-Marin M, Lima S, Matinha-Cardoso J, Tamagnini P, Oliveira P . Isolation and Characterization of Cyanobacterial Extracellular Vesicles. J Vis Exp. 2022; (180). DOI: 10.3791/63481. View

Qiu G, Jiang H, Lis H, Li Z, Deng B, Shang J . A unique porin meditates iron-selective transport through cyanobacterial outer membranes. Environ Microbiol. 2020; 23(1):376-390. DOI: 10.1111/1462-2920.15324. View

Rast A, Schaffer M, Albert S, Wan W, Pfeffer S, Beck F . Biogenic regions of cyanobacterial thylakoids form contact sites with the plasma membrane. Nat Plants. 2019; 5(4):436-446. DOI: 10.1038/s41477-019-0399-7. View

Biller S, Lundeen R, Hmelo L, Becker K, Arellano A, Dooley K . Prochlorococcus extracellular vesicles: molecular composition and adsorption to diverse microbes. Environ Microbiol. 2021; 24(1):420-435. PMC: 9298688. DOI: 10.1111/1462-2920.15834. View

10.

Wang P, Ji S, Grimm B . Post-translational regulation of metabolic checkpoints in plant tetrapyrrole biosynthesis. J Exp Bot. 2022; 73(14):4624-4636. PMC: 9992760. DOI: 10.1093/jxb/erac203. View

11.

Usui K, Yamamoto H, Oi T, Taniguchi M, Mori H, Fujita Y . Extracellular Vesicle-Mediated Secretion of Protochlorophyllide in the Cyanobacterium . Plants (Basel). 2022; 11(7). PMC: 9003413. DOI: 10.3390/plants11070910. View

12.

Hiraide Y, Oshima K, Fujisawa T, Uesaka K, Hirose Y, Tsujimoto R . Loss of cytochrome cM stimulates cyanobacterial heterotrophic growth in the dark. Plant Cell Physiol. 2014; 56(2):334-45. DOI: 10.1093/pcp/pcu165. View

13.

Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y . Identification of two homologous genes, chlAI and chlAII, that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem. 2007; 283(5):2684-92. DOI: 10.1074/jbc.M708954200. View

14.

Kojima S, Muramoto K, Kusano T . Outer Membrane Proteins Derived from Non-cyanobacterial Lineage Cover the Peptidoglycan of Cyanophora paradoxa Cyanelles and Serve as a Cyanelle Diffusion Channel. J Biol Chem. 2016; 291(38):20198-209. PMC: 5025702. DOI: 10.1074/jbc.M116.746131. View

15.

Robey R, Steadman K, Polgar O, Morisaki K, Blayney M, Mistry P . Pheophorbide a is a specific probe for ABCG2 function and inhibition. Cancer Res. 2004; 64(4):1242-6. DOI: 10.1158/0008-5472.can-03-3298. View

16.

Reinbothe C, El Bakkouri M, Buhr F, Muraki N, Nomata J, Kurisu G . Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction. Trends Plant Sci. 2010; 15(11):614-24. DOI: 10.1016/j.tplants.2010.07.002. View

17.

Fujita Y, Matsumoto H, Takahashi Y, Matsubara H . Identification of a nifDK-like gene (ORF467) involved in the biosynthesis of chlorophyll in the cyanobacterium Plectonema boryanum. Plant Cell Physiol. 1993; 34(2):305-14. View

18.

Westphal S, Heins L, Soll J, Vothknecht U . Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis?. Proc Natl Acad Sci U S A. 2001; 98(7):4243-8. PMC: 31210. DOI: 10.1073/pnas.061501198. View

19.

Fujita Y . Protochlorophyllide reduction: a key step in the greening of plants. Plant Cell Physiol. 1996; 37(4):411-21. DOI: 10.1093/oxfordjournals.pcp.a028962. View

20.

Kim J, Lee J, Park J, Gho Y . Gram-negative and Gram-positive bacterial extracellular vesicles. Semin Cell Dev Biol. 2015; 40:97-104. DOI: 10.1016/j.semcdb.2015.02.006. View