Genome Sequence and Transcriptome Analyses of Chrysochromulina tobin: Metabolic Tools for Enhanced Algal Fitness in the Prominent Order Prymnesiales (Haptophyceae)

PLoS Genetics

Volumn 11, Issue 9, 2015, Pages

  Hovde, Blake T ^a   Deodato, Chloe R ^a   Hunsperger, Heather M ^a   Ryken, Scott A ^a   Yost, Will ^a   Jha, Ramesh K ^b   Patterson, Johnathan ^a   Monnat, Raymond J ^a   Barlow, Steven B ^c   Starkenburg, Shawn R ^b   Cattolico, Rose Ann ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MACROLIDE; MEMBRANE PROTEIN; MULTIDRUG AND TOXIC COMPOUND EXTRUSION PROTEIN; NONRIBOSOMAL PEPTIDE SYNTHASE GENE; NONRIBOSOMAL PEPTIDE SYNTHETASE; POLYKETIDE SYNTHASE; POLYPEPTIDE ANTIBIOTIC AGENT; RHODOPSIN; RIBULOSEBISPHOSPHATE CARBOXYLASE; UNCLASSIFIED DRUG; XANTHORHODOPSIN;

ARTICLE; CELL GROWTH; CHLOROPLAST GENOME; CHRYSOCHROMULINA TOBIN; CONTROLLED STUDY; FATTY ACID SYNTHESIS; GENE EXPRESSION; GENE SEQUENCE; HAPTOPHYTA; HORIZONTAL GENE TRANSFER; HOST RESISTANCE; LIPID DEGRADATION; LIPOGENESIS; MITOCHONDRIAL GENOME; NONHUMAN; PHOTOPERIODICITY; POLYKETIDE SYNTHASE GENE; PRYMNESIALES; TRANSCRIPTOMICS; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; GENOME; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; REPRODUCTIVE FITNESS;

BASE SEQUENCE; GENE EXPRESSION PROFILING; GENETIC FITNESS; GENOME; HAPTOPHYTA; MOLECULAR SEQUENCE ANNOTATION; PHYLOGENY; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SEQUENCE ANALYSIS, DNA;

EID: 84943520818     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005469     Document Type: Article

References (123)

1. Kirkham AR, Lepère C, Jardillier LE, Not F, Bouman H, Mead A, et al. A global perspective on marine photosynthetic picoeukaryote community structure. ISME J. 2013;7: 922–936. doi: 10.1038/ismej.2012.166 23364354
2. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P, Primary production of the biosphere: Integrating terrestrial and oceanic components. Science. 1998;281: 237–240. 9657713
3. Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12: e1001889. doi: 10.1371/journal.pbio.1001889 24959919
4. Medlin LK, Sáez AG, Young JR, A molecular clock for coccolithophores and implications for selectivity of phytoplankton extinctions across the K/T boundary. Mar Micropaleontol. 2008;67: 69–86.
5. Shiraiwa Y, Physiological regulation of carbon fixation in the photosynthesis and calcification of coccolithophorids. Comp Biochem Physiol B Biochem Mol Biol. 2003;136: 775–783. 14662302
6. Li C, Yang G, Pan J, Zhang H, Experimental studies on dimethylsulfide (DMS) and dimethylsulfoniopropionate (DMSP) production by four marine microalgae. Acta Oceanol Sin. 2010;29: 78–87.
7. John U, Beszteri S, Glöckner G, Singh R, Medlin L, Cembella AD, Genomic characterisation of the ichthyotoxic prymnesiophyte Chrysochromulina polylepis, and the expression of polyketide synthase genes in synchronized cultures. Eur J Phycol. 2010;45: 215–229.
8. Alderkamp A-C, Buma AGJ, Rijssel van M, Leeuwe MA van, Stefels J, Belviso S, Lancelot C, Verity PG, Gieskes WWC, The carbohydrates of Phaeocystis and their degradation in the microbial food web. In: Phaeocystis, major link in the biogeochemical cycling of climate-relevant elements. Springer Netherlands; 2007. pp. 99–118. http://link.springer.com/chapter/10.1007/978-1-4020-6214-8_9
9. Hemaiswarya S, Raja R, Kumar RR, Ganesan V, Anbazhagan C, Microalgae: a sustainable feed source for aquaculture. World J Microbiol Biotechnol. 2011;27: 1737–1746.
10. Simon M, López-García P, Moreira D, Jardillier L, New haptophyte lineages and multiple independent colonizations of freshwater ecosystems. Environ Microbiol Rep. 2013;5: 322–332. doi: 10.1111/1758-2229.12023 23584973
11. Bittner L, Gobet A, Audic S, Romac S, Egge ES, Santini S, et al. Diversity patterns of uncultured haptophytes unravelled by pyrosequencing in Naples Bay. Mol Ecol. 2013;22: 87–101. doi: 10.1111/mec.12108 23163508
12. Liu H, Probert I, Uitz J, Claustre H, Aris-Brosou S, Frada M, et al. Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. Proc Natl Acad Sci U S A. 2009;106: 12803–12808. doi: 10.1073/pnas.0905841106 19622724
13. Shalchian-Tabrizi K, Reier-Røberg K, Ree DK, Klaveness D, Bråte J, Marine-freshwater colonizations of haptophytes inferred from phylogeny of environmental 18S rDNA sequences. J Eukaryot Microbiol. 2011;58: 315–318. doi: 10.1111/j.1550-7408.2011.00547.x 21518078
14. Jones HLJ, Leadbeater BSC, Green JC, Mixotrophy in haptophytes. The Haptophyte Algae. Oxford: Clarendon Press; 1994. pp. 247–264.
15. Edvardsen B, Eikrem W, Throndsen J, Sáez AG, Probert I, Medlin LK, Ribosomal DNA phylogenies and a morphological revision provide the basis for a revised taxonomy of the Prymnesiales (Haptophyta). Eur J Phycol. 2011;46: 202–228.
16. Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, et al. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature. 2013;499: 209–213. doi: 10.1038/nature12221 23760476
17. Marsh ME, Regulation of CaCO3 formation in coccolithophores. Comp Biochem Physiol B Biochem Mol Biol. 2003;136: 743–754. 14662299
18. Holligan PM, Viollier M, Harbour DS, Camus P, Champagne-Philippe M, Satellite and ship studies of coccolithophore production along a continental shelf edge. Nature. 1983;304: 339–342.
19. Von Dassow P, John U, Ogata H, Probert I, Bendif EM, Kegel JU, et al. Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton. ISME J. 2014.
20. McDonald S., Sarno D, Scanlan D., Zingone A, Genetic diversity of eukaryotic ultraphytoplankton in the Gulf of Naples during an annual cycle. Aquat Microb Ecol. 2007;50: 75–89.
21. Egge ES, Eikrem W, Edvardsen B, Deep-branching novel lineages and high diversity of haptophytes in the Skagerrak (Norway) uncovered by 454 pyrosequencing. J Eukaryot Microbiol. 2015;62: 121–140. doi: 10.1111/jeu.12157 25099994
22. Bigelow N, Barker J, Ryken S, Patterson J, Hardin W, Barlow S, et al. Chrysochromulina sp.: A proposed lipid standard for the algal biofuel industry and its application to diverse taxa for screening lipid content. Algal Res. 2013;2: 385–393.
23. Jordan RW, Chamberlain AHL, Biodiversity among haptophyte algae. Biodivers Conserv. 1997;6: 131–152.
24. Stiller JW, Schreiber J, Yue J, Guo H, Ding Q, Huang J, The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat Commun. 2014;5.
25. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, et al. The tree of eukaryotes. Trends Ecol Evol. 2005;20: 670–676. 16701456
26. Wang D, Ning K, Li J, Hu J, Han D, Wang H, et al. Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet. 2014;10: e1004094. doi: 10.1371/journal.pgen.1004094 24415958
27. Vaulot D, Birrien J-L, Marie D, Casotti R, Veldhuis MJW, Kraay GW, et al. Morphology, ploidy, pigment composition, and genome size of cultured strains of Phaeocystis (prymnesiophyceae). J Phycol. 1994;30: 1022–1035.
28. Green JC, Course PA, Tarran GA, The life-cycle of Emiliania huxleyi: A brief review and a study of relative ploidy levels analysed by flow cytometry. J Mar Syst. 1996;9: 33–44.
29. Hunsperger HM, Randhawa T, Cattolico RA, Extensive horizontal gene transfer, duplication, and loss of chlorophyll synthesis genes in the algae. BMC Evol Biol. 2015;15: 16. doi: 10.1186/s12862-015-0286-4 25887237
30. Hovde BT, Starkenburg SR, Hunsperger HM, Mercer LD, Deodato CR, Jha RK, et al. The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles. BMC Genomics. 2014;15: 604. doi: 10.1186/1471-2164-15-604 25034814
31. Guo Z, Zhang H, Lin S, Light-promoted rhodopsin expression and starvation survival in the marine dinoflagellate Oxyrrhis marina. PloS One. 2014;9: e114941. doi: 10.1371/journal.pone.0114941 25506945
32. Padilla GM, Genetic expression in the cell cycle. Elsevier; 2012.
33. Sforza E, Simionato D, Giacometti GM, Bertucco A, Morosinotto T, Adjusted light and dark cycles can optimize photosynthetic efficiency in algae growing in photobioreactors. PLoS ONE. 2012;7.
34. Ragni M, D’Alcala M, Circadian variability in the photobiology of Phaeodactylum tricornutum: pigment content. J Plankton Res. 2007; 141–156.
35. Rost B, Riebesell U, Sültemeyer D, Carbon acquisition of marine phytoplankton: Effect of photoperiod length. Limnol Oceanogr. 2006;51: 12–20.
36. Trentacoste EM, Shrestha RP, Smith SR, Glé C, Hartmann AC, Hildebrand M, et al. Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth. Proc Natl Acad Sci U S A. 2013;110: 19748–19753. doi: 10.1073/pnas.1309299110 24248374
37. Radakovits R, Jinkerson RE, Darzins A, Posewitz MC, Genetic engineering of algae for enhanced biofuel production. Eukaryot Cell. 2010;9: 486–501. doi: 10.1128/EC.00364-09 20139239
38. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, et al. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J Cell Mol Biol. 2008;54: 621–639.
39. Jeffery SW, Brown MR, Volkman JK, Haptophytes as feedstocks in mariculture. The Haptophyte Algae. Oxford: Clarendon Press; 1994. pp. 287–302.
40. Lee S, Seo CH, Lim B, Yang JO, Oh J, Kim M, et al. Accurate quantification of transcriptome from RNA-Seq data by effective length normalization. Nucleic Acids Res. 2011;39: e9. doi: 10.1093/nar/gkq1015 21059678
41. Bigelow NW, Hardin WR, Barker JP, Ryken SA, Macrae AC, Cattolico RA, A comprehensive GC-MS sub-microscale assay for fatty acids and its applications. J Am Oil Chem Soc. 2011;88: 1329–1338. 21909157
42. Manning SR, La Claire JW, Prymnesins: Toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Mar Drugs. 2010;8: 678–704. doi: 10.3390/md8030678 20411121
43. Staunton J, Weissman KJ, Polyketide biosynthesis: a millennium review. Nat Prod Rep. 2001;18: 380–416. 11548049
44. Shen B, Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol. 2003;7: 285–295. 12714063
45. Etchegaray A, Rabello E, Dieckmann R, Moon DH, Fiore MF, Döhren von H, et al. Algicide production by the filamentous cyanobacterium Fischerella sp. CENA 19. J Appl Phycol. 2004;16: 237–243. doi: 10.1023/B:JAPH.0000048509.77816.5e
46. Finking R, Marahiel MA, Biosynthesis of nonribosomal peptides. Annu Rev Microbiol. 2004;58: 453–488. 15487945
47. Du L, Sánchez C, Shen B, Hybrid peptide-polyketide natural products: biosynthesis and prospects toward engineering novel molecules. Metab Eng. 2001;3: 78–95. 11162234
48. Aron ZD, Dorrestein PC, Blackhall JR, Kelleher NL, Walsh CT, Characterization of a new tailoring domain in polyketide biogenesis: the amine transferase domain of MycA in the mycosubtilin gene cluster. J Am Chem Soc. 2005;127: 14986–14987. 16248612
49. Fisch KM, Biosynthesis of natural products by microbial iterative hybrid PKS–NRPS. RSC Adv. 2013;3: 18228–18247.
50. Sondergaard TE, Hansen FT, Purup S, Nielsen AK, Bonefeld-Jørgensen EC, Giese H, et al. Fusarin C acts like an estrogenic agonist and stimulates breast cancer cells in vitro. Toxicol Lett. 2011;205: 116–121. doi: 10.1016/j.toxlet.2011.05.1029 21683775
51. Gelderblom WC, Thiel PG, Jaskiewicz K, Marasas WF, Investigations on the carcinogenicity of fusarin C—a mutagenic metabolite of Fusarium moniliforme. Carcinogenesis. 1986;7: 1899–1901. 2876785
52. Maiya S, Grundmann A, Li X, Li S-M, Turner G, Identification of a hybrid PKS/NRPS required for pseurotin A biosynthesis in the human pathogen Aspergillus fumigatus. Chembiochem Eur J Chem Biol. 2007;8: 1736–1743.
53. Masschelein J, Mattheus W, Gao L-J, Moons P, Van Houdt R, Uytterhoeven B, et al. A PKS/NRPS/FAS hybrid gene cluster from Serratia plymuthica RVH1 encoding the biosynthesis of three broad spectrum, zeamine-related antibiotics. PloS One. 2013;8: e54143. doi: 10.1371/journal.pone.0054143 23349809
54. Hamilton-Miller JM, Chemistry and biology of the polyene macrolide antibiotics. Bacteriol Rev. 1973;37: 166–196. 4202146
55. Fouces R, Mellado E, Díez B, Barredo JL, The tylosin biosynthetic cluster from Streptomyces fradiae: genetic organization of the left region. Microbiol Read Engl. 1999;145 (Pt 4): 855–868.
56. Cundliffe E, Bate N, Butler A, Fish S, Gandecha A, Merson-Davies L, The tylosin-biosynthetic genes of Streptomyces fradiae. Antonie Van Leeuwenhoek. 2001;79: 229–234. 11816964
57. Baltz RH, Seno ET, Stonesifer J, Wild GM, Biosynthesis of the macrolide antibiotic tylosin. A preferred pathway from tylactone to tylosin. J Antibiot (Tokyo). 1983;36: 131–141.
58. Morar M, Pengelly K, Koteva K, Wright GD, Mechanism and diversity of the erythromycin esterase family of enzymes. Biochemistry (Mosc). 2012;51: 1740–1751.
59. Miura K, Ueno S, Kamiya K, Kobayashi J, Matsuoka H, Ando K, et al. Cloning of mRNA sequences for two antibacterial peptides in a hemipteran insect, Riptortus clavatus. Zoolog Sci. 1996;13: 111–117. 8688805
60. Thomas S, Karnik S, Barai RS, Jayaraman VK, Idicula-Thomas S, CAMP: a useful resource for research on antimicrobial peptides. Nucleic Acids Res. 2010;38: D774–780. doi: 10.1093/nar/gkp1021 19923233
61. Torrent M, Nogués MV, Boix E, Discovering new in silico tools for antimicrobial peptide prediction. Curr Drug Targets. 2012;13: 1148–1157. 22664076
62. Sims JJ, Donnell MS, Leary JV, Lacy GH, Antimicrobial agents from marine algae. Antimicrob Agents Chemother. 1975;7: 320–321. 1137385
63. Al-Saif SSA, Abdel-Raouf N, El-Wazanani HA, Aref IA, Antibacterial substances from marine algae isolated from Jeddah coast of Red sea, Saudi Arabia. Saudi J Biol Sci. 2014;21: 57–64. doi: 10.1016/j.sjbs.2013.06.001 24596500
64. Sun X, Gilroy EM, Chini A, Nurmberg PL, Hein I, Lacomme C, et al. ADS1 encodes a MATE-transporter that negatively regulates plant disease resistance. New Phytol. 2011;192: 471–482. doi: 10.1111/j.1469-8137.2011.03820.x 21762165
65. Jin Y, Nair A, van Veen HW, Multidrug transport protein norM from Vibrio cholerae simultaneously couples to sodium- and proton-motive force. J Biol Chem. 2014;289: 14624–14632. doi: 10.1074/jbc.M113.546770 24711447
66. Omote H, Hiasa M, Matsumoto T, Otsuka M, Moriyama Y, The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci. 2006;27: 587–593. 16996621
67. Eckardt NA, Move it on out with MATEs. Plant Cell. 2001;13: 1477–1480. 11449044
68. Rodríguez-Beltrán J, Rodríguez-Rojas A, Guelfo JR, Couce A, Blázquez J, The Escherichia coli SOS gene dinF protects against oxidative stress and bile salts. PloS One. 2012;7: e34791. doi: 10.1371/journal.pone.0034791 22523558
69. Slamovits CH, Okamoto N, Burri L, James ER, Keeling PJ, A bacterial proteorhodopsin proton pump in marine eukaryotes. Nat Commun. 2011;2: 183. doi: 10.1038/ncomms1188 21304512
70. Kazamia E, Czesnick H, Nguyen TTV, Croft MT, Sherwood E, Sasso S, et al. Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ Microbiol. 2012;14: 1466–1476. doi: 10.1111/j.1462-2920.2012.02733.x 22463064
71. Ruiz-González MX, Marín I, New insights into the evolutionary history of type 1 rhodopsins. J Mol Evol. 2004;58: 348–358. 15045490
72. Bamann C, Bamberg E, Wachtveitl J, Glaubitz C, Proteorhodopsin. Biochim Biophys Acta. 2014;1837: 614–625. doi: 10.1016/j.bbabio.2013.09.010 24060527
73. Riedel T, Gómez-Consarnau L, Tomasch J, Martin M, Jarek M, González JM, et al. Genomics and physiology of a marine flavobacterium encoding a proteorhodopsin and a xanthorhodopsin-like protein. PloS One. 2013;8: e57487. doi: 10.1371/journal.pone.0057487 23526944
74. Béjà O, Lanyi JK, Nature’s toolkit for microbial rhodopsin ion pumps. Proc Natl Acad Sci U S A. 2014;111: 6538–6539. doi: 10.1073/pnas.1405093111 24737891
75. Luecke H, Schobert B, Stagno J, Imasheva ES, Wang JM, Balashov SP, et al. Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore. Proc Natl Acad Sci U S A. 2008;105: 16561–16565. doi: 10.1073/pnas.0807162105 18922772
76. Mongodin EF, Nelson KE, Daugherty S, Deboy RT, Wister J, Khouri H, et al. The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci U S A. 2005;102: 18147–18152. 16330755
77. Shand RF, Betlach MC, Expression of the bop gene cluster of Halobacterium halobium is induced by low oxygen tension and by light. J Bacteriol. 1991;173: 4692–4699. 1856168
78. Sharma AK, Spudich JL, Doolittle WF, Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol. 2006;14: 463–469. 17008099
79. Wisecaver JH, Hackett JD, Dinoflagellate genome evolution. Annu Rev Microbiol. 2011;65: 369–387. doi: 10.1146/annurev-micro-090110-102841 21682644
80. Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S, Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol Mol Biol Rev MMBR. 2007;71: 576–599. 18063718
81. Boczar BA, Delaney TP, Cattolico RA, Gene for the ribulose-1,5-bisphosphate carboxylase small subunit protein of the marine chromophyte Olisthodiscus luteus is similar to that of a chemoautotrophic bacterium. Proc Natl Acad Sci U S A. 1989;86: 4996–4999. 2740337
82. Newman SM, Cattolico RA, Structural, functional, and evolutionary analysis of ribulose-1,5-bisphosphate carboxylase from the chromophytic alga Olisthodiscus luteus. Plant Physiol. 1987;84: 483–490. 16665466
83. Portis AR, Rubisco activase—Rubisco’s catalytic chaperone. Photosynth Res. 2003;75: 11–27. 16245090
84. Maier UG, Fraunholz M, Zauner S, Penny S, Douglas S, A nucleomorph-encoded CbbX and the phylogeny of RuBisCo regulators. Mol Biol Evol. 2000;17: 576–583. 10742049
85. Zarzycki J, Axen SD, Kinney JN, Kerfeld CA, Cyanobacterial-based approaches to improving photosynthesis in plants. J Exp Bot. 2013;64: 787–798. doi: 10.1093/jxb/ers294 23095996
86. Fujita K, Tanaka K, Sadaie Y, Ohta N, Functional analysis of the plastid and nuclear encoded CbbX proteins of Cyanidioschyzon merolae. Genes Genet Syst. 2008;83: 135–142. 18506097
87. Starkenburg SR, Kwon KJ, Jha RK, McKay C, Jacobs M, Chertkov O, et al. A pangenomic analysis of the Nannochloropsis organellar genomes reveals novel genetic variations in key metabolic genes. BMC Genomics. 2014;15: 212. doi: 10.1186/1471-2164-15-212 24646409
88. Mueller-Cajar O, Stotz M, Wendler P, Hartl FU, Bracher A, Hayer-Hartl M, Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase. Nature. 2011;479: 194–199. doi: 10.1038/nature10568 22048315
89. Whitney SM, Houtz RL, Alonso H, Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiol. 2011;155: 27–35. doi: 10.1104/pp.110.164814 20974895
90. Helliwell KE, Wheeler GL, Leptos KC, Goldstein RE, Smith AG, Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Mol Biol Evol. 2011;28: 2921–2933. doi: 10.1093/molbev/msr124 21551270
91. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG, Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature. 2005;438: 90–93. 16267554
92. Koid AE, Liu Z, Terrado R, Jones AC, Caron DA, Heidelberg KB, Comparative transcriptome analysis of four prymnesiophyte algae. PloS One. 2014;9: e97801. doi: 10.1371/journal.pone.0097801 24926657
93. Oudot-Le Secq M-P, Green BR, Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Gene. 2011;476: 20–26. doi: 10.1016/j.gene.2011.02.001 21320580
94. Kim E, Lane CE, Curtis BA, Kozera C, Bowman S, Archibald JM, Complete sequence and analysis of the mitochondrial genome of Hemiselmis andersenii CCMP644 (Cryptophyceae). BMC Genomics. 2008;9: 215. doi: 10.1186/1471-2164-9-215 18474103
95. Zerbino DR, Birney E, Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18: 821–829. doi: 10.1101/gr.074492.107 18349386
96. Holt C, Yandell M, MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics. 2011;12: 491. doi: 10.1186/1471-2105-12-491 22192575
97. Smit A, Hubley, R, Green, P. RepeatMasker Open-3.0 [Internet]. 2010. http://www.repeatmasker.org
98. Trapnell C, Pachter L, Salzberg SL, TopHat: discovering splice junctions with RNA-Seq. Bioinforma Oxf Engl. 2009;25: 1105–1111.
99. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28: 511–515. doi: 10.1038/nbt.1621 20436464
100. Parra G, Bradnam K, Korf I, CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinforma Oxf Engl. 2007;23: 1061–1067.
101. Stanke M, Schöffmann O, Morgenstern B, Waack S, Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics. 2006;7: 62. 16469098
102. Korf I, Gene finding in novel genomes. BMC Bioinformatics. 2004;5: 59. 15144565
103. Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M, Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 2008;18: 1979–1990. doi: 10.1101/gr.081612.108 18757608
104. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M, Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinforma Oxf Engl. 2005;21: 3674–3676.
105. Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A, et al. Manipulation of FASTQ data with Galaxy. Bioinforma Oxf Engl. 2010;26: 1783–1785.
106. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5: 621–628. doi: 10.1038/nmeth.1226 18516045
107. Raivo Kolde. pheatmap: Pretty Heatmaps. R package [Internet]. http://CRAN.R-project.org/package=pheatmap
108. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29: 644–652. doi: 10.1038/nbt.1883 21572440
109. Jochem FJ, Dark survival strategies in marine phytoplankton assessed by cytometric measurement of metabolic activity with fluorescein diacetate. Mar Biol. 1999;135: 721–728.
110. Raman S, Vernon R, Thompson J, Tyka M, Sadreyev R, Pei J, et al. Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins. 2009;77 Suppl 9: 89–99. doi: 10.1002/prot.22540 19701941
111. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, Jacak R, Michael L, Johnson Ludwig Brand, et al. Chapter nineteen—Rosetta3: an object-oriented software suite for the simulation and design of macromolecules. In: Methods in Enzymology. Academic Press; 2011. pp. 545–574. doi: 10.1016/B978-0-12-381270-4.00019-6 21187238
112. O’Meara MJ, Leaver-Fay A, Tyka M, Stein A, Houlihan K, DiMaio F, et al. A combined covalent-electrostatic model of hydrogen bonding improves structure prediction with Rosetta. J Chem Theory Comput. 2015.
113. Jones DT, Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol. 1999;292: 195–202. 10493868
114. Kim DE, Chivian D, Baker D, Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 2004;32: W526–W531. 15215442
115. Hanwell MD, Curtis DE, Lonie DC, Vandermeersch T, Zurek E, Hutchison GR, Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. J Cheminformatics. 2012;4: 17.
116. Rohl CA, Strauss CEM, Misura KMS, Baker D, Protein structure prediction using Rosetta. Methods Enzymol. 2004;383: 66–93. 15063647
117. Davis IW, Baker D, RosettaLigand Docking with Full Ligand and Receptor Flexibility. J Mol Biol. 2009;385: 381–392. doi: 10.1016/j.jmb.2008.11.010 19041878
118. Edgar RC, MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32: 1792–1797. 15034147
119. Abascal F, Zardoya R, Posada D, ProtTest: selection of best-fit models of protein evolution. Bioinforma Oxf Engl. 2005;21: 2104–2105.
120. Posada D, jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25: 1253–1256. doi: 10.1093/molbev/msn083 18397919
121. Ronquist F, Huelsenbeck JP, MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19: 1572–1574. 12912839
122. Drummond AJ, Suchard MA, Xie D, Rambaut A, Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29: 1969–1973. doi: 10.1093/molbev/mss075 22367748
123. Stamatakis A, RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22: 2688–2690. 16928733