Elucidation of the whole carotenoid biosynthetic pathway of aphids at the gene level and arthropodal food chain involving aphids and the red dragonfly

BMC Zoology - Tập 6 - Trang 1-13 - 2021
Miho Takemura1, Takashi Maoka1,2, Takashi Koyanagi3, Naoki Kawase4, Ritsuo Nishida5, Tsutomu Tsuchida6, Mantaro Hironaka7, Tetsuyuki Ueda8, Norihiko Misawa1
1Research Institute for Bioresources and Biotechnology, Ishikawa Prefectural University, Nonoichi-shi, Japan
2Research Institute for Production Development, Sakyo-ku, Japan
3Department of Food Science, Ishikawa Prefectural University, Nonoichi-shi, Japan
4Minakuchi Kodomono-mori Nature Museum, Koka-shi, Japan
5Emeritus Prof., Kyoto University, Sakyo-ku, Japan
6Faculty of Science, Academic Assembly, University of Toyama, Toyama, Japan
7Department of Production Science, Ishikawa Prefectural University, Nonoichi-shi, Japan
8Emeritus Prof., Ishikawa Prefectural University, Nonoichi-shi, Japan

Tóm tắt

Aphids can be positioned as robust pest insects in farming and as ones of the model organisms for arthropods in molecular biology. Carotenoids are pigments that protect organisms from photooxidative damage caused by excessive light. Aphids were shown to possess genes of fungal origin for carotenoid biosynthesis, whereas a little knowledge was available about the functions of the genes and the biosynthetic pathway. Even carotenoid species contained in aphids were not enough understood. Main purpose of this study is to clarify these insufficient findings. The whole carotenoid biosynthetic pathway of the pea aphid (Acyrthosiphon pisum) was elucidated at the gene level, through comprehensive functional analysis of its carotenogenic genes, using Escherichia coli that synthesized carotenoid substrates, along with structural and quantitative analysis of carotenoids from various aphid species. Four genes were needed to synthesize all carotenoids accumulated in aphids from geranylgeranyl diphosphate. The tor gene mediated desaturation reaction from phytoene to 3,4-didehydrolycopene. It was revealed that a gene designated ApCrtYB3, which was considered to have functionally evolved in aphids, can convert lycopene into uncommon carotenoids with the γ-ring such as (6′S)-β,γ-carotene and γ,γ-carotene. We further demonstrated that the atypical carotenoids work as ecological indicators for estimating the food chain from aphids to predatory arthropods, and showed that aphids contributed with significant levels to the food chain from insect herbivores to several predatory arthropods, i.e., the red dragonfly (Sympetrum frequens; adults), seven-spotted ladybird (Coccinella septempunctata), and two spiders, Oxyopes sertatus and Nephila clavata. Gut microflora of the dragonfly (mature adults) was also found to include endosymbiotic bacteria such as Serratia symbiotica specific to the black bean aphid (Aphis fabae). We revealed the whole carotenoid biosynthetic pathway of aphids, including functional identification of the corresponding genes. Subsequently, we showed that arthropodal food chain can be estimated using the uncommon carotenoids of aphids as ecological indicators. This result indicated that aphids made significant contributions to the food chain of several predatory arthropods including the red-dragonfly adults. Aphids are likely to be positioned as an important “phytochemicals” source for some predatory insects and arachnids, which are often active under bright sunlight.

Tài liệu tham khảo

Frank HA, Cogdell RJ. The photochemistry and function of carotenoids in photosynthesis. In: Young AJ, Britton G, editors. Carotenoids in photosynthesis. Dordrecht: Springer; 1993. p. 252–326. https://doi.org/10.1007/978-94-011-2124-8_8. Stahl W, Site H. Bioactivity and protective effects of natural carotenoids. Biochim Biophys Acta. 1740;2004:101–7. Britton G, Liaaen-Jensen S, Pfander H. Carotenoids handbook. Basel: Birkhäuser Verlag; 2004. https://doi.org/10.1007/978-3-0348-7836-4. Misawa N. Carotenoids. In: Mander L, Lui HW, editors. Comprehensive natural products II chemistry and biology Vol. 1. Oxford: Elsevier; 2010. p. 733–53. Moise AR, Al-Babili S, Wutzel ET. Mechanistic aspects of carotenoid biosynthesis. Chem Rev. 2014;114(1):164–93. https://doi.org/10.1021/cr400106y. Moran NA, Jarvik T. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science. 2010;328(5978):624–7. https://doi.org/10.1126/science.1187113. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. 2011;479(7374):487–92. https://doi.org/10.1038/nature10640. Cobbs C, Heath J, Stireman JO III, Abbot P. Carotenoids in unexpected places: gall midges, lateral gene transfer, and carotenoid biosynthesis in animals. Mol Phylogenet Evol. 2013;68(2):221–8. https://doi.org/10.1016/j.ympev.2013.03.012. Nováková E, Moran NA. Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. Mol Biol Evol. 2012;29(1):313–23. https://doi.org/10.1093/molbev/msr206. Zhao C, Nabity PD. Phylloxerids share ancestral carotenoid biosynthesis genes of fungal origin with aphids and adelgids. PLoS One. 2017;12(10):e0185484. https://doi.org/10.1371/journal.pone.0185484. Zhang L, Wang MY, Li XP, Wang XT, Jia CL, Yang XZ, et al. A small set of differentially expressed genes was associated with two color morphs in natural populations of the pea aphid Acyrthosiphon pisum. Gene. 2018;651:23–32. https://doi.org/10.1016/j.gene.2018.01.079. Ding BY, Niu J, Shang F, Yang L, Zhang W, Smagghe G, et al. Parental silencing of a horizontally transferred carotenoid desaturase gene causes a reduction of red pigment and fitness in the pea aphid. Pest Manag Sci. 2020;76(7):2423–33. https://doi.org/10.1002/ps.5783. Bryon A, Kurlovs AH, Dermauw W, Greenhalgh R, Riga M, Grbić M, et al. Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae. Proc Natl Acad Sci U S A. 2017;114(29):E5871–80. https://doi.org/10.1073/pnas.1706865114. Wybouw N, Kurlovs AH, Greenhalgh R, Bryon A, Kosterlitz O, Manabe Y, et al. Convergent evolution of cytochrome P450s underlies independent origins of keto-carotenoid pigmentation in animals. Proc R Soc B Biol Sci. 2019;286(1907):20191039. https://doi.org/10.1098/rspb.2019.1039. Veeman A. Carotenoid metabolism in Tetranychus urticae Koch (Acari; Tetranychidae). Comp Biochem Physiol. 1974;47B:101–16. Goodwin TW. Arachnids and insects. In: Goodwin TW, editor. The biochemistry of the carotenoids. Vol. II animals. London: Chapman and Hall; 1984. p. 97–121. Andrewes AG, Kjosen H, Liaaen-Jensen S, Weisgraber KH, Lousberg RJ, Weiss U. Animal carotenoids. 7. Carotenes of two colour variants of the aphid Macrosiphum liliodendri – identification of natural γ,γ-carotene. Acta Chem Scand. 1971;25(10):3878–80. https://doi.org/10.3891/acta.chem.scand.25-3878. Jenkins RL, Loxdale HD, Brookes CP, Dixon AFG. The major carotenoid pigments of the grain aphid, Sitobion avenae (F.) (Hemiptera: Aphididae). Physiol Entomol. 1999;24(2):171–8. https://doi.org/10.1046/j.1365-3032.1999.00128.x. Ding BY, Niu J, Shang F, Yang L, Chang TY, Wang JJ. Characterization of the geranylgeranyl diphosphate gene in Acyrthosiphon pisum (Hemiptera: Aphididae) and its association with carotenoid biosynthesis. Front Physiol. 2019;10:1398. https://doi.org/10.3389/fphys.2019.01398. Britton G, Goodwin TW, Harriman GE, Lockley WJS. Carotenoids of the ladybird beetle; Coccinella septempunctata. Insect Biochem. 1977;7(4):337–45. https://doi.org/10.1016/0020-1790(77)90035-X. Asahina S. The development of odonatology in the Far East. Odonatologica. 1974;3:5–12. Corbet PS. Portrait: Sympetrum frequens. In: Corbet PS, editor. Dragonflies: behavior and ecology of Odonata. New York: Cornell University Press; 1999. p. 390–2. Maoka T, Kawase N, Ueda T, Nishida R. Carotenoids of dragonflies, from the perspective of comparative biochemical and chemical ecological studies. Biochem Syst Ecol. 2020;89:104001. https://doi.org/10.1016/j.bse.2020.104001. Schmidhauser TJ, Lauter FR, Russo VE, Yanofsky C. Cloning, sequence, and photoregulation of al-1, a carotenoid biosynthetic gene of Neurospora crassa. Mol Cell Biol. 1990;10(10):5064–70. https://doi.org/10.1128/MCB.10.10.5064. Verdoes JC, Misawa N, van Ooyen AJJ. Cloning and characterization of the astaxanthin biosynthetic gene encoding phytoene desaturase of Xanthophyllomyces dendrorhous. Biotechnol Bioeng. 1999;63(6):750–5. https://doi.org/10.1002/(SICI)1097-0290(19990620)63:6<750::AID-BIT13>3.0.CO;2-7. Verdoes JC, Krubasik P, Sandmann G, van Ooyen AJJ. Isolation and functional characterization of a novel type of carotenoid biosynthetic gene from Xanthophyllomyces dendrorhous. Mol Gen Genet. 1999;262(3):453–61. https://doi.org/10.1007/s004380051105. Hausmann A, Sandmann G. A single five-step desaturase is involved in the carotenoid biosynthesis pathway to β-carotene and torulene in Neurospora crassa. Fungal Genet Biol. 2000;30(2):147–53. https://doi.org/10.1006/fgbi.2000.1212. Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, et al. Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol. 1990;172(12):6704–12. https://doi.org/10.1128/JB.172.12.6704-6712.1990. Linden H, Misawa N, Chamovitz D, Pecker I, Hirschberg J, Sandmann G. Functional complementation in Escherichia coli of different phytoene desaturase genes and analysis of accumulated carotenes. Z Naturforsch. 1991;46c:1045–51. Schmidt-Dannert C, Umeno D, Arnold FH. Molecular breeding of carotenoid biosynthetic pathway. Nat Biotechnol. 2000;18(7):750–3. https://doi.org/10.1038/77319. Lehner A, Grimm M, Rattei T, Ruepp A, Frishman D, Manzardo GG, et al. Cloning and characterization of Enterobacter sakazakii pigment genes and in situ spectroscopic analysis of the pigment. FEMS Microbiol Lett. 2006;265(2):244–8. https://doi.org/10.1111/j.1574-6968.2006.00500.x. Sedkova N, Tao L, Rouvière PE, Cheng Q. Diversity of carotenoid synthesis gene clusters from environmental Enterobacteriaceae strains. Appl Environ Microbiol. 2005;71(12):8141–6. https://doi.org/10.1128/AEM.71.12.8141-8146.2005. Choi SK, Osawa A, Maoka T, Hattan J, Ito K, Uchiyama A, et al. 3-β-Glucosyl-3′-β-quinovosyl zeaxanthin, a novel carotenoid glycoside synthesized by Escherichia coli cells expressing the Pantoea ananatis carotenoid biosynthesis gene cluster. Appl Microbiol Biotechnol. 2013;97(19):8479–86. https://doi.org/10.1007/s00253-013-5101-9. Fukaya Y, Takemura M, Koyanagi T, Maoka T, Shindo K, Misawa N. Structural and functional analysis of the carotenoid biosynthesis genes of a Pseudomonas strain isolated from the excrement of Autumn Darter. Biosci Biotechnol Biochem. 2018;82(6):1043–52. https://doi.org/10.1080/09168451.2017.1398069. Sabri A, Leroy P, Haubruge E, Hance T, Frère I, Destain J, et al. Isolation, pure culture and characterization of Serratia symbiotica sp. nov., the R-type of secondary endosymbiont of the black bean aphid Aphis fabae. Int J Syst Evol Microbiol. 2011;61(Pt 9):2081–8. https://doi.org/10.1099/ijs.0.024133-0. Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, et.al. Symbiotic bacterium modifies aphid body color. Science. 2010;330:1102–1104, 6007, DOI: https://doi.org/10.1126/science.1195463. Duron O, Hurst GDD. Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biol. 2013;11(1):45. https://doi.org/10.1186/1741-7007-11-45. Johnson CG. The composition of aerial populations and the vertical distribution of insects in the air. In: Johnson CG, editor. Migration and dispersal of insects by flight. London: Methuen & Co Ltd; 1969. p. 294–360. Misawa N, Satomi Y, Kondo K, Yokoyama A, Kajiwara S, Saito T, et al. Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J Bacteriol. 1995;177(22):6575–84. https://doi.org/10.1128/JB.177.22.6575-6584.1995. Kajiwara S, Fraser PD, Kondo K, Misawa N. Expression of an exogenous isopentenyl diphosphate isomerase gene enhances isoprenoid biosynthesis in Escherichia coli. Biochem J. 1997;324(2):421–6. https://doi.org/10.1042/bj3240421. Takemura M, Maoka T, Misawa N. Biosynthetic routes of hydroxylated carotenoids (xanthophylls) in Marchantia polymorpha (liverwort), and production of novel and rare xanthophylls through pathway engineering in Escherichia coli. Planta. 2015;241(3):699–710. https://doi.org/10.1007/s00425-014-2213-0. Rose RE. The nucleotide sequence of pACYC184. Nucleic Acids Res. 1988;16(1):355. https://doi.org/10.1093/nar/16.1.355. Takemura M, Kubo A, Higuchi Y, Maoka T, Sahara T, Yaoi K, et al. Pathway engineering for efficient biosynthesis of violaxanthin in Escherichia coli. Appl Microbiol Biotechnol. 2019;103(23-24):9393–9. https://doi.org/10.1007/s00253-019-10182-w. Takemura M, Maoka T, Misawa N. Carotenoid analysis of a liverwort Marchantia polymorpha and functional identification of its lycopene β- and ε-cyclase genes. Plant Cell Physiol. 2014;55(1):194–200. https://doi.org/10.1093/pcp/pct170. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. https://doi.org/10.1038/nmeth.f.303. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261–7. https://doi.org/10.1128/AEM.00062-07. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–72. https://doi.org/10.1128/AEM.03006-05.