Genomes Reveal Evolution of Microalgal Oleaginous Traits
Oleaginous microalgae are promising feedstock for biofuels, yet the genetic diversity, origin and evolution of oleaginous traits remain largely unknown. Here we present a detailed phylogenomic analysis of five oleaginous Nannochloropsis species (a total of six strains) and one time-series transcriptome dataset for triacylglycerol (TAG) synthesis on one representative strain. Despite small genome sizes, high coding potential and relative paucity of mobile elements, the genomes feature small cores of ca. 2,700 protein-coding genes and a large pan-genome of >38,000 genes. The six genomes share key oleaginous traits, such as the enrichment of selected lipid biosynthesis genes and certain glycoside hydrolase genes that potentially shift carbon flux from chrysolaminaran to TAG synthesis. The eleven type II diacylglycerol acyltransferase genes (DGAT-2) in every strain, each expressed during TAG synthesis, likely originated from three ancient genomes, including the secondary endosymbiosis host and the engulfed green and red algae. Horizontal gene transfers were inferred in most lipid synthesis nodes with expanded gene doses and many glycoside hydrolase genes. Thus multiple genome pooling and horizontal genetic exchange, together with selective inheritance of lipid synthesis genes and species-specific gene loss, have led to the enormous genetic apparatus for oleaginousness and the wide genomic divergence among present-day Nannochloropsis. These findings have important implications in the screening and genetic engineering of microalgae for biofuels.
Vyšlo v časopise:
Genomes Reveal Evolution of Microalgal Oleaginous Traits. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004094
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004094
Souhrn
Oleaginous microalgae are promising feedstock for biofuels, yet the genetic diversity, origin and evolution of oleaginous traits remain largely unknown. Here we present a detailed phylogenomic analysis of five oleaginous Nannochloropsis species (a total of six strains) and one time-series transcriptome dataset for triacylglycerol (TAG) synthesis on one representative strain. Despite small genome sizes, high coding potential and relative paucity of mobile elements, the genomes feature small cores of ca. 2,700 protein-coding genes and a large pan-genome of >38,000 genes. The six genomes share key oleaginous traits, such as the enrichment of selected lipid biosynthesis genes and certain glycoside hydrolase genes that potentially shift carbon flux from chrysolaminaran to TAG synthesis. The eleven type II diacylglycerol acyltransferase genes (DGAT-2) in every strain, each expressed during TAG synthesis, likely originated from three ancient genomes, including the secondary endosymbiosis host and the engulfed green and red algae. Horizontal gene transfers were inferred in most lipid synthesis nodes with expanded gene doses and many glycoside hydrolase genes. Thus multiple genome pooling and horizontal genetic exchange, together with selective inheritance of lipid synthesis genes and species-specific gene loss, have led to the enormous genetic apparatus for oleaginousness and the wide genomic divergence among present-day Nannochloropsis. These findings have important implications in the screening and genetic engineering of microalgae for biofuels.
Zdroje
1. WijffelsRH, BarbosaMJ (2010) An outlook on microalgal biofuels. Science 329: 796–799.
2. GeorgiannaDR, MayfieldSP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488: 329–335.
3. WangD, LuY, HuangH, XuJ (2012) Establishing oleaginous microalgae research models for consolidated bioprocessing of solar energy. Adv Biochem Eng Biotechnol 128: 69–84.
4. KilianO, BenemannCS, NiyogiKK, VickB (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc Natl Acad Sci USA 108: 21265–21269.
5. RadakovitsR, JinkersonRE, FuerstenbergSI, TaeH, SettlageRE, et al. (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropsis gaditana. Nat Commun 3: 686.
6. VielerA, WuGX, TsaiCH, BullardB, CornishAJ, et al. (2012) Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet 8: e1003064.
7. MerchantSS, ProchnikSE, VallonO, HarrisEH, KarpowiczSJ, et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250.
8. ArmbrustEV, BergesJA, BowlerC, GreenBR, MartinezD, et al. (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79–86.
9. ParkerMS, MockT, ArmbrustEV (2008) Genomic insights into marine microalgae. Annu Rev Genet 42: 619–645.
10. WallDP, HirshAE, FraserHB, KummJ, GiaeverG, et al. (2005) Functional genomic analysis of the rates of protein evolution. Proc Natl Acad Sci USA 102: 5483–5488.
11. MataJ, BahlerJ (2003) Correlations between gene expression and gene conservation in fission yeast. Genome Res 13: 2686–2690.
12. JordanIK, RogozinIB, WolfYI, KooninEV (2002) Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 12: 962–968.
13. ChenF, MackeyAJ, StoeckertCJ, RoosDS (2006) OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 34: 363–368.
14. MatsuzakiM, MisumiO, Shin-IT, MaruyamaS, TakaharaM, et al. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657.
15. MoustafaA, BeszteriB, MaierUG, BowlerC, ValentinK, et al. (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324: 1724–1726.
16. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189.
17. Jenke-KodamaH, SandmannA, MullerR, DittmannE (2005) Evolutionary implications of bacterial polyketide synthases. Mol Biol Evol 22: 2027–2039.
18. SchonknechtG, ChenWH, TernesCM, BarbierGG, ShresthaRP, et al. (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339: 1207–1210.
19. PascualF, CarmanGM (2013) Phosphatidate phosphatase, a key regulator of lipid homeostasis. BBA-Mol Cell Biol L 1831: 514–522.
20. HuQ, SommerfeldM, JarvisE, GhirardiM, PosewitzM, et al. (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54: 621–639.
21. Turchetto-ZoletA, MaraschinF, de MoraisG, CagliariA, AndradeC, et al. (2011) Evolutionary view of acyl-CoA diacylglycerol acyltransferase (DGAT), a key enzyme in neutral lipid biosynthesis. BMC Evol Bio 11: 263.
22. ChanCX, Reyes-PrietoA, BhattacharyaD (2011) Red and green algal origin of diatom membrane transporters: insights into environmental adaptation and cell evolution. PLoS One 6: e29138.
23. Cavalier-SmithT (1999) Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46: 347–366.
24. CurtisBA, TanifujiG, BurkiF, GruberA, IrimiaM, et al. (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492: 59–65.
25. MayerW, SchusterL, BartelmesG, DieterichC, SommerR (2011) Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC Evol Biol 11: 13.
26. FalkowskiPG, KatzME, KnollAH, QuiggA, RavenJA, et al. (2004) The evolution of modern eukaryotic phytoplankton. Science 305: 354–360.
27. KrylovDM, WolfYI, RogozinIB, KooninEV (2003) Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res 13: 2229–2235.
28. DeschampsP, MoreiraD (2012) Reevaluating the green contribution to diatom genomes. Genome Biol Evol 4: 795–800.
29. BhattacharyaD, PriceDC, ChanCX, QiuH, RoseN, et al. (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4: 1941.
30. AnderssonDI, HughesD (2009) Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 43: 167–195.
31. SandegrenL, AnderssonDI (2009) Bacterial gene amplification: implications for the evolution of antibiotic resistance. Nat Rev Microbiol 7: 578–588.
32. ZhouZ, GuJ, LiYQ, WangY (2012) Genome plasticity and systems evolution in Streptomyces. BMC Bioinformatics 13: S8.
33. AmesRM, RashBM, HentgesKE, RobertsonDL, DelneriD, et al. (2010) Gene duplication and environmental adaptation within yeast populations. Genome Biol Evol 2: 591–601.
34. PanG, XuJ, LiT, XiaQ, LiuSL, et al. (2013) Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 14: 186.
35. BartosJ, VlcekC, ChouletF, DzunkovaM, CvikovaK, et al. (2012) Intraspecific sequence comparisons reveal similar rates of non-collinear gene insertion in the B and D genomes of bread wheat. BMC Plant Biol 12: 155.
36. Cardoso-MoreiraM, EmersonJJ, ClarkAG, LongMY (2011) Drosophila duplication hotspots are associated with late-replicating regions of the genome. PLoS Genet 7: e1002340.
37. DongHP, WilliamsE, WangDZ, XieZX, HsiaRC, et al. (2013) Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiol 162: 1110–1126.
38. CollenJ, PorcelB, CarreW, BallSG, ChaparroC, et al. (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci USA 110: 5247–5252.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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