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Volume 10, Issue 4

Chromosome-scale assembly of the streamlined picoeukaryote sp. SENEW3 genome reveals Rabl-like chromatin structure and potential for C photosynthesis Open Access

Abstract

Genome sequencing and assembly of the photosynthetic picoeukaryotic sp. SENEW3 revealed a compact genome with a reduced gene set, few repetitive sequences, and an organized Rabl-like chromatin structure. Hi-C chromosome conformation capture revealed evidence of possible chromosomal translocations, as well as putative centromere locations. Maintenance of a relatively few selenoproteins, as compared to similarly sized marine picoprasinophytes Mamiellales, and broad halotolerance compared to others in Trebouxiophyceae, suggests evolutionary adaptation to variable salinity environments. Such adaptation may have driven size and genome minimization and have been enabled by the retention of a high number of membrane transporters. Identification of required pathway genes for both CAM and C photosynthetic carbon fixation, known to exist in the marine mamiellale pico-prasinophytes and seaweed , but few other chlorophyte species, further highlights the unique adaptations of this robust alga. This high-quality assembly provides a significant advance in the resources available for genomic investigations of this and other photosynthetic picoeukaryotes.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): C4photosynthesis , chromatin structure , environmental adaption , genomic assembly , Photosynthetic picoeukaryote and Picochlorum
Funding
This study was supported by the:
  • ARC Centre of Excellence in Synthetic Biology (Award CE200100029)
    • Principle Award Recipient: IanT. Paulsen
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-04-29
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References

  1. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H et al. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 2012; 31:1–46 [View Article]
     [Google Scholar]
  2. Leliaert F, Tronholm A, Lemieux C, Turmel M, DePriest MS et al. Chloroplast phylogenomic analyses reveal the deepest-branching lineage of the Chlorophyta, Palmophyllophyceae class. nov. Sci Rep 2016; 6:25367 [View Article] [PubMed]
     [Google Scholar]
  3. Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A et al. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 2012; 13:R39 [View Article] [PubMed]
     [Google Scholar]
  4. Hirooka S, Hirose Y, Kanesaki Y, Higuchi S, Fujiwara T et al. Acidophilic green algal genome provides insights into adaptation to an acidic environment. Proc Natl Acad Sci U S A 2017; 114:E8304–E8313 [View Article] [PubMed]
     [Google Scholar]
  5. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 2012; 335:843–847 [View Article] [PubMed]
     [Google Scholar]
  6. Suzuki S, Endoh R, Manabe R-I, Ohkuma M, Hirakawa Y. Multiple losses of photosynthesis and convergent reductive genome evolution in the colourless green algae Prototheca. Sci Rep 2018; 8:940 [View Article] [PubMed]
     [Google Scholar]
  7. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007; 318:245–250 [View Article] [PubMed]
     [Google Scholar]
  8. Featherston J, Arakaki Y, Hanschen ER, Ferris PJ, Michod RE et al. The 4-celled Tetrabaena socialis nuclear genome reveals the essential components for genetic control of cell number at the origin of multicellularity in the volvocine lineage. Mol Biol Evol 2018; 35:855–870 [View Article] [PubMed]
     [Google Scholar]
  9. Worden AZ, Lee J-H, Mock T, Rouzé P, Simmons MP et al. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 2009; 324:268–272 [View Article] [PubMed]
     [Google Scholar]
  10. Roth MS, Cokus SJ, Gallaher SD, Walter A, Lopez D et al. Chromosome-level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production. Proc Natl Acad Sci U S A 2017; 114:E4296–E4305 [View Article] [PubMed]
     [Google Scholar]
  11. Potter D, Lajeunesse TC, Saunders GW, Anderson RA. Convergent evolution masks extensive biodiversity among marine coccoid picoplankton. Biodivers Conserv 1997; 6:99–107 [View Article]
     [Google Scholar]
  12. de Vargas C, Audic S, Henry N, Decelle J, Mahé F et al. Eukaryotic plankton diversity in the sunlit ocean. Science 2015; 348:1261605 [View Article] [PubMed]
     [Google Scholar]
  13. Vaulot D, Eikrem W, Viprey M, Moreau H. The diversity of small eukaryotic phytoplankton (≤3 μm) in marine ecosystems. FEMS Microbiol Rev 2008; 32:795–820 [View Article] [PubMed]
     [Google Scholar]
  14. Caron DA, Countway PD, Jones AC, Kim DY, Schnetzer A. Marine protistan diversity. Ann Rev Mar Sci 2012; 4:467–493 [View Article] [PubMed]
     [Google Scholar]
  15. Metz S, Lopes Dos Santos A, Berman MC, Bigeard E, Licursi M et al. Diversity of photosynthetic picoeukaryotes in eutrophic shallow lakes as assessed by combining flow cytometry cell-sorting and high throughput sequencing. FEMS Microbiol Ecol 2019; 95:fiz038 [View Article] [PubMed]
     [Google Scholar]
  16. Wang F, Xie Y, Wu W, Sun P, Wang L et al. Picoeukaryotic diversity and activity in the northwestern Pacific Ocean Based on rDNA and rRNA high-throughput sequencing. Front Microbiol 2018; 9:3259 [View Article] [PubMed]
     [Google Scholar]
  17. Raven JA. The twelfth Tansley Lecture. Small is beautiful: the picophytoplankton. Funct. Ecol. 1998; 12:503–513 [View Article]
     [Google Scholar]
  18. Fouilland E, Descolas-Gros C, Courties C, Collos Y, Vaquer A et al. Productivity and growth of a natural population of the smallest free-living eukaryote under nitrogen deficiency and sufficiency. Microb Ecol 2004; 48:103–110 [View Article] [PubMed]
     [Google Scholar]
  19. Butcher RW. Contributions to our knowledge of the smaller marine algae. J Mar Biol Ass 1952; 31:175–191 [View Article]
     [Google Scholar]
  20. Henley WJ, Hironaka JL, Guillou L, Buchheim MA, Buchheim JA et al. Phylogenetic analysis of the ‘Nannochloris-like’ algae and diagnoses of Picochlorum oklahomensis gen. et sp. nov. (Trebouxiophyceae, Chlorophyta). Phycologia 2004; 43:641–652 [View Article]
     [Google Scholar]
  21. da Roza PA, Goold HD, Paulsen IT. Picochlorum sp. SENEW3. Trends Genet 2021 [View Article] [PubMed]
     [Google Scholar]
  22. Blanc-Mathieu R, Verhelst B, Derelle E, Rombauts S, Bouget F-Y et al. An improved genome of the model marine alga Ostreococcus tauri unfolds by assessing Illumina de novo assemblies. BMC Genomics 2014; 15:1103 [View Article] [PubMed]
     [Google Scholar]
  23. Derelle E, Ferraz C, Rombauts S, Rouzé P, Worden AZ et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A 2006; 103:11647–11652 [View Article] [PubMed]
     [Google Scholar]
  24. Palenik B, Grimwood J, Aerts A, Rouzé P, Salamov A et al. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci U S A 2007; 104:7705–7710 [View Article] [PubMed]
     [Google Scholar]
  25. Blanc-Mathieu R, Krasovec M, Hebrard M, Yau S, Desgranges E et al. Population genomics of picophytoplankton unveils novel chromosome hypervariability. Sci Adv 2017; 3:e1700239 [View Article] [PubMed]
     [Google Scholar]
  26. Foflonker F, Price DC, Qiu H, Palenik B, Wang S et al. Genome of the halotolerant green alga Picochlorum sp. reveals strategies for thriving under fluctuating environmental conditions. Environ Microbiol 2015; 17:412–426 [View Article] [PubMed]
     [Google Scholar]
  27. Wang S, Lambert W, Giang S, Goericke R, Palenik B. Microalgal assemblages in a poikilohaline pond. J Phycol 2014; 50:303–309 [View Article] [PubMed]
     [Google Scholar]
  28. Foflonker F, Ananyev G, Qiu H, Morrison A, Palenik B et al. The unexpected extremophile: tolerance to fluctuating salinity in the green alga Picochlorum. Algal Res. 2016; 16:465–472 [View Article]
     [Google Scholar]
  29. Weissman JC, Likhogrud M, Thomas DC, Fang W, Karns DAJ et al. High-light selection produces a fast-growing Picochlorum celeri. Algal Res. 2018; 36:17–28 [View Article]
     [Google Scholar]
  30. Watanabe K, Fujii K. Isolation of high-level-CO2 -preferring Picochlorum sp. strains and their biotechnological potential. Algal Res. 2016; 18:135–143 [View Article]
     [Google Scholar]
  31. Foflonker F. Understanding the Genomic Basis of Stress Adaptation in Picochlorum Green Algae 2018
     [Google Scholar]
  32. Hazeem LJ, Bououdina M, Rashdan S, Brunet L, Slomianny C et al. Cumulative effect of zinc oxide and titanium oxide nanoparticles on growth and chlorophyll a content of Picochlorum sp. Environ Sci Pollut Res Int 2016; 23:2821–2830 [View Article] [PubMed]
     [Google Scholar]
  33. Dimier C, Corato F, Saviello G, Brunet C. Photophysiological properties of the marine picoeukaryote Picochlorum RCC 237 (Trebouxiophyceae, Chlorophyta)1. J Phycol 2007; 43:275–283 [View Article]
     [Google Scholar]
  34. Dogaris I, Brown TR, Loya B, Philippidis G. Cultivation study of the marine microalga Picochlorum oculatum and outdoor deployment in a novel bioreactor for high-density production of algal cell mass. Biomass Bioenergy 2016; 89:11–23 [View Article]
     [Google Scholar]
  35. Dahmen I, Chtourou H, Jebali A, Daassi D, Karray F et al. Optimisation of the critical medium components for better growth of Picochlorum sp. and the role of stressful environments for higher lipid production. J Sci Food Agric 2014; 94:1628–1638 [View Article] [PubMed]
     [Google Scholar]
  36. El-Kassas HY. Growth and fatty acid profile of the marine microalga Picochlorum sp. grown under nutrient stress conditions. Egypt. J. Aquat. Res. 2013; 39:233–239 [View Article]
     [Google Scholar]
  37. Tanhaemami M, Alizadeh E, Sanders CK, Marrone BL, Munsky B. Using flow cytometry and multistage machine learning to discover label-free signatures of algal lipid accumulation. Phys Biol 2019; 16:055001 [View Article] [PubMed]
     [Google Scholar]
  38. Tran D, Giordano M, Louime C, Tran N, Vo T et al. An isolated Picochlorum species for aquaculture, food, and biofuel. N American J Aquac 2014; 76:305–311 [View Article]
     [Google Scholar]
  39. de la Vega M, Díaz E, Vila M, León R. Isolation of a new strain of Picochlorum sp and characterization of its potential biotechnological applications. Biotechnol Prog 2011; 27:1535–1543 [View Article] [PubMed]
     [Google Scholar]
  40. Yang F, Xiang W, Sun X, Wu H, Li T et al. A novel lipid extraction method from wet microalga Picochlorum sp. at room temperature. Mar Drugs 2014; 12:1258–1270 [View Article] [PubMed]
     [Google Scholar]
  41. Edmundson SJ, Huesemann MH. The dark side of algae cultivation: characterizing night biomass loss in three photosynthetic algae, Chlorella sorokiniana, Nannochloropsis salina and Picochlorum sp. Algal Res. 2015; 12:470–476 [View Article]
     [Google Scholar]
  42. Dinesh Kumar S, Santhanam P, Nandakumar R, Ananth S, Nithya P et al. Bioremediation of shrimp (Litopenaeus Vannamei) cultured effluent using Copepod (Oithona Rigida) and Microalgae (Picochlorum maculatam & Amphora sp.)—An integrated approach. Desalin Water Treat 2016; 57:26257–26266 [View Article]
     [Google Scholar]
  43. Chen T-Y, Lin H-Y, Lin C-C, Lu C-K, Chen Y-M. Picochlorum as an alternative to Nannochloropsis for grouper larval rearing. Aquaculture 2012; 338–341:82–88 [View Article]
     [Google Scholar]
  44. Dinesh Kumar S, Santhanam P, Ananth S, Kaviyarasan M, Nithya P et al. Evaluation of suitability of wastewater-grown microalgae (Picochlorum maculatum) and copepod (Oithona rigida) as live feed for white leg shrimp Litopenaeus vannamei post-larvae. Aquacult Int 2017; 25:393–411 [View Article]
     [Google Scholar]
  45. Dinesh Kumar S, Santhanam P, Prabhavathi P, Kanimozhi B, Abirami M et al. Optimal conditions for the treatment of shrimp culture effluent using immobilized marine microalga Picochlorum maculatum (PSDK01). Proc Natl Acad Sci, India, Sect B Biol Sci 2018; 88:1177–1185 [View Article]
     [Google Scholar]
  46. von Alvensleben N, Stookey K, Magnusson M, Heimann K. Salinity tolerance of Picochlorum atomus and the use of salinity for contamination control by the freshwater cyanobacterium Pseudanabaena limnetica. PLoS One 2013; 8:e63569 [View Article] [PubMed]
     [Google Scholar]
  47. Dahlin LR, Gerritsen AT, Henard CA, Van Wychen S, Linger JG et al. Development of a high-productivity, halophilic, thermotolerant microalga Picochlorum renovo. Commun Biol 2019; 2:388 [View Article] [PubMed]
     [Google Scholar]
  48. Dahlin LR, Guarnieri MT. Development of the high-productivity marine microalga, Picochlorum renovo, as a photosynthetic protein secretion platform. Algal Res. 2021; 54:102197 [View Article]
     [Google Scholar]
  49. Gonzalez-Esquer CR, Wright KT, Sudasinghe N, Carr CK, Sanders CK et al. Demonstration of the potential of Picochlorum soloecismus as a microalgal platform for the production of renewable fuels. Algal Res. 2019; 43:101658 [View Article]
     [Google Scholar]
  50. Krishnan A, Likhogrud M, Cano M, Edmundson S, Melanson JB et al. Picochlorum celeri as a model system for robust outdoor algal growth in seawater. Sci Rep 2021; 11:11649 [View Article] [PubMed]
     [Google Scholar]
  51. Barten R, van Workum D-JM, de Bakker E, Risse J, Kleisman M et al. Genetic mechanisms underlying increased microalgal thermotolerance, maximal growth rate, and yield on light following adaptive laboratory evolution. BMC Biol 2022; 20:242 [View Article] [PubMed]
     [Google Scholar]
  52. Foflonker F, Mollegard D, Ong M, Yoon HS, Bhattacharya D. Genomic analysis of Picochlorum species reveals how microalgae may adapt to variable environments. Mol Biol Evol 2018; 35:2702–2711 [View Article] [PubMed]
     [Google Scholar]
  53. Venkatesan BM, Bashir R. Nanopore sensors for nucleic acid analysis. Nat Nanotechnol 2011; 6:615–624 [View Article] [PubMed]
     [Google Scholar]
  54. Rhoads A, Au KF. PacBio sequencing and its applications. Genom Proteom Bioinform 2015; 13:278–289 [View Article] [PubMed]
     [Google Scholar]
  55. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science 2002; 295:1306–1311 [View Article] [PubMed]
     [Google Scholar]
  56. Belton J-M, McCord RP, Gibcus JH, Naumova N, Zhan Y et al. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods 2012; 58:268–276 [View Article] [PubMed]
     [Google Scholar]
  57. Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO et al. A chromosome conformation capture ordered sequence of the barley genome. Nature 2017; 544:427–433 [View Article] [PubMed]
     [Google Scholar]
  58. van Berkum NL, Lieberman-Aiden E, Williams L, Imakaev M, Gnirke A et al. Hi-C: a method to study the three-dimensional architecture of genomes. J Vis Exp 201039 [View Article] [PubMed]
     [Google Scholar]
  59. Oluwadare O, Highsmith M, Cheng J. An overview of methods for reconstructing 3-d chromosome and genome structures from Hi-C data. Biol Proced Online 2019; 21:7 [View Article] [PubMed]
     [Google Scholar]
  60. Brůna T, Hoff KJ, Lomsadze A, Stanke M, Borodovsky M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom Bioinform 2021; 3:lqaa108 [View Article] [PubMed]
     [Google Scholar]
  61. Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv 2012
     [Google Scholar]
  62. Cantarel BL, Korf I, Robb SMC, Parra G, Ross E et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 2008; 18:188–196 [View Article] [PubMed]
     [Google Scholar]
  63. Holt C, Yandell M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 2011; 12:491 [View Article] [PubMed]
     [Google Scholar]
  64. Pham GM, Hamilton JP, Wood JC, Burke JT, Zhao H et al. Construction of a chromosome-scale long-read reference genome assembly for potato. Gigascience 2020; 9:giaa100 [View Article] [PubMed]
     [Google Scholar]
  65. Wang J, Liu W, Zhu D, Hong P, Zhang S et al. Chromosome-scale genome assembly of sweet cherry (Prunus avium L.) cv. Tieton obtained using long-read and Hi-C sequencing. Hortic Res 2020; 7:122 [View Article] [PubMed]
     [Google Scholar]
  66. Ma D, Guo Z, Ding Q, Zhao Z, Shen Z et al. Chromosome-level assembly of the mangrove plant Aegiceras corniculatum genome generated through Illumina, PacBio and Hi-C sequencing technologies. Mol Ecol Resour 2021; 21:1593–1607 [View Article] [PubMed]
     [Google Scholar]
  67. Guillard RR, Ryther JH. Studies of marine planktonic diatoms. Can J Microbiol 1962; 8:229–239
     [Google Scholar]
  68. Guillard RRL. Culture of phytoplankton for feeding marine invertebrates. In Smith WL, Chanley MH. eds Culture of Marine Invertebrate Animals: Proceedings — 1st Conference on Culture of Marine Invertebrate Animals Greenport Boston, MA: Springer US; 1975 pp 29–60 [View Article]
     [Google Scholar]
  69. Keller MD, Selvin RC, Claus W, Guillard RRL. Media for the culture of oceanic ultraphytoplankton. J Phycol 1987; 23:633–638
     [Google Scholar]
  70. Sanchez F, Geffroy S, Norest M, Yau S, Moreau H et al. Simplified transformation of Ostreococcus tauri using polyethylene glycol. Genes 2019; 10:399 [View Article] [PubMed]
     [Google Scholar]
  71. Hage AE, Houseley J. Resolution of budding yeast chromosomes using pulsed-field gel electrophoresis. In Makovets S. eds DNA Electrophoresis (Methods in Molecular Biology (Methods and Protocols) Totowa, NJ: Humana Press; 2013 pp 195–207 [View Article]
     [Google Scholar]
  72. Sambrook J, Russell DW, Irwin CA, Laboratory CSH, Fund R et al. Molecular Cloning: A Laboratory Manual, 3rd ed Cold Spring Harbor Laboratory Press; 2001
     [Google Scholar]
  73. Jagielski T, Gawor J, Bakuła Z, Zuchniewicz K, Żak I et al. An optimized method for high quality DNA extraction from microalga Prototheca wickerhamii for genome sequencing. Plant Methods 2017; 13:77 [View Article] [PubMed]
     [Google Scholar]
  74. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Müller WEG et al. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 2004; 14:1147–1159 [View Article] [PubMed]
     [Google Scholar]
  75. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
     [Google Scholar]
  76. Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res 2017; 27:737–746 [View Article] [PubMed]
     [Google Scholar]
  77. Medaka: Sequence correction provided by ONT Research; 2018 https://github.com/nanoporetech/medaka
  78. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
     [Google Scholar]
  79. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. Gigascience 2021; 10:giab008 [View Article] [PubMed]
     [Google Scholar]
  80. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  81. Bonfield JK, Whitwham A. Gap5--editing the billion fragment sequence assembly. Bioinformatics 2010; 26:1699–1703 [View Article] [PubMed]
     [Google Scholar]
  82. Servant N, Varoquaux N, Lajoie BR, Viara E, Chen C-J et al. HiC-Pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol 2015; 16:259 [View Article] [PubMed]
     [Google Scholar]
  83. Abdennur N, Mirny LA. Cooler: scalable storage for Hi-C data and other genomically labeled arrays. Bioinformatics 2020; 36:311–316 [View Article]
     [Google Scholar]
  84. Hunter JD. Matplotlib: a 2D graphics environment. Comput Sci Eng 2007; 9:90–95 [View Article]
     [Google Scholar]
  85. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  86. Stanke M, Waack S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 2003; 19 Suppl 2:ii215–25 [View Article] [PubMed]
     [Google Scholar]
  87. Keller O, Odronitz F, Stanke M, Kollmar M, Waack S. Scipio: using protein sequences to determine the precise exon/intron structures of genes and their orthologs in closely related species. BMC Bioinformatics 2008; 9:278 [View Article] [PubMed]
     [Google Scholar]
  88. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31:3210–3212 [View Article] [PubMed]
     [Google Scholar]
  89. Korf I. Gene finding in novel genomes. BMC Bioinformatics 2004; 5:59 [View Article] [PubMed]
     [Google Scholar]
  90. Lomsadze A, Ter-Hovhannisyan V, Chernoff YO, Borodovsky M. Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res 2005; 33:6494–6506 [View Article] [PubMed]
     [Google Scholar]
  91. Campbell MS, Law M, Holt C, Stein JC, Moghe GD et al. MAKER-P: a tool kit for the rapid creation, management, and quality control of plant genome annotations. Plant Physiol. 2013; 164:513–524 [View Article]
     [Google Scholar]
  92. Gonzalez-Esquer CR, Twary SN, Hovde BT, Starkenburg SR. Nuclear, chloroplast, and mitochondrial genome sequences of the prospective microalgal biofuel strain Picochlorum soloecismus. Genome Announc 2018; 6:e01498-17 [View Article] [PubMed]
     [Google Scholar]
  93. Coordinators NR. Database resources of the national center for biotechnology information. Nucleic Acids Res 2018; 46:D8–d13
     [Google Scholar]
  94. Consortium TU. Uniprot: a worldwide hub of protein knowledge. Nucleic Acids Res. 2018; 47:D506–D515
     [Google Scholar]
  95. Blum M, Chang H-Y, Chuguransky S, Grego T, Kandasaamy S et al. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res 2021; 49:D344–D354 [View Article] [PubMed]
     [Google Scholar]
  96. Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 2016; 44:W54–7 [View Article] [PubMed]
     [Google Scholar]
  97. Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. In Kollmar M. eds Gene Prediction Methods in Molecular Biology New York, NY: Humana; 2019 pp 227–245 [View Article]
     [Google Scholar]
  98. Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci U S A 2020; 117:9451–9457 [View Article] [PubMed]
     [Google Scholar]
  99. Tarailo-Graovac M, Chen N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics 2009; Chapter 4:4 [View Article] [PubMed]
     [Google Scholar]
  100. Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 2019; 20:238 [View Article] [PubMed]
     [Google Scholar]
  101. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 2015; 16:157 [View Article] [PubMed]
     [Google Scholar]
  102. Yin Y, Mao X, Yang J, Chen X, Mao F et al. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2012; 40:W445–51 [View Article] [PubMed]
     [Google Scholar]
  103. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article] [PubMed]
     [Google Scholar]
  104. Elbourne LDH, Tetu SG, Hassan KA, Paulsen IT. TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life. Nucleic Acids Res 2017; 45:D320–D324 [View Article] [PubMed]
     [Google Scholar]
  105. Weiß CL, Pais M, Cano LM, Kamoun S, Burbano HA. nQuire: a statistical framework for ploidy estimation using next generation sequencing. BMC Bioinformatics 2018; 19:122 [View Article] [PubMed]
     [Google Scholar]
  106. Ranallo-Benavidez TR, Jaron KS, Schatz MC. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun 2020; 11:1432 [View Article] [PubMed]
     [Google Scholar]
  107. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article] [PubMed]
     [Google Scholar]
  108. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article] [PubMed]
     [Google Scholar]
  109. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
     [Google Scholar]
  110. Engel SR, Dietrich FS, Fisk DG, Binkley G, Balakrishnan R et al. The reference genome sequence of Saccharomyces cerevisiae: then and now. G3 Genes/Genomes/Genetics 2014; 4:389–398 [View Article] [PubMed]
     [Google Scholar]
  111. Lynch M, Walsh B. The Origins of Genome Architecture: Sinauer Associates Sunderland, MA 2007
     [Google Scholar]
  112. Gaut BS, Ross-Ibarra J. Selection on major components of angiosperm genomes. Science 2008; 320:484–486 [View Article] [PubMed]
     [Google Scholar]
  113. Leliaert F. Green algae: chlorophyta and streptophyta. In Schmidt TM. eds Encyclopedia of Microbiology (Fourth Edition) Oxford: Academic Press; 2019 pp 457–468
     [Google Scholar]
  114. Schurko AM, Logsdon JM. Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex. Bioessays 2008; 30:579–589 [View Article] [PubMed]
     [Google Scholar]
  115. Hofstatter PG, Ribeiro GM, Porfírio‐Sousa AL, Lahr DJG. The sexual ancestor of all eukaryotes: a defense of the “meiosis toolkit.”. BioEssays 2020; 42: [View Article] [PubMed]
     [Google Scholar]
  116. Morris JJ, Lenski RE, Zinser ER. The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 2012; 3:e00036–00012 [View Article] [PubMed]
     [Google Scholar]
  117. Wolf YI, Koonin EV. Genome reduction as the dominant mode of evolution. Bioessays 2013; 35:829–837 [View Article] [PubMed]
     [Google Scholar]
  118. Derilus D, Rahman MZ, Pinero F, Massey SE. Synergism between the Black Queen effect and the proteomic constraint on genome size reduction in the photosynthetic picoeukaryotes. Sci Rep 2020; 10:8918 [View Article] [PubMed]
     [Google Scholar]
  119. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009; 326:289–293 [View Article] [PubMed]
     [Google Scholar]
  120. Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 2014; 159:1665–1680 [View Article] [PubMed]
     [Google Scholar]
  121. Marie-Nelly H, Marbouty M, Cournac A, Flot J-F, Liti G et al. High-quality genome (re)assembly using chromosomal contact data. Nat Commun 2014; 5:5695 [View Article] [PubMed]
     [Google Scholar]
  122. Burton JN, Adey A, Patwardhan RP, Qiu R, Kitzman JO et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol 2013; 31:1119–1125 [View Article] [PubMed]
     [Google Scholar]
  123. Kaplan N, Dekker J. High-throughput genome scaffolding from in vivo DNA interaction frequency. Nat Biotechnol 2013; 31:1143–1147 [View Article] [PubMed]
     [Google Scholar]
  124. Shan T, Yuan J, Su L, Li J, Leng X et al. First genome of the brown alga Undaria pinnatifida: chromosome-level assembly using PacBio and Hi-C technologies. Front Genet 2020; 11:140 [View Article] [PubMed]
     [Google Scholar]
  125. Chen H, Chu JS-C, Chen J, Luo Q, Wang H et al. Insights into the ancient adaptation to intertidal environments by red algae based on a genomic and multiomics investigation of Neoporphyra haitanensis. Mol Biol Evol 2022; 39:msab315 [View Article] [PubMed]
     [Google Scholar]
  126. Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J et al. Earth biogenome project: sequencing life for the future of life. Proc Natl Acad Sci U S A 2018; 115:4325–4333 [View Article] [PubMed]
     [Google Scholar]
  127. Zhou Y, Shearwin-Whyatt L, Li J, Song Z, Hayakawa T et al. Platypus and echidna genomes reveal mammalian biology and evolution. Nature 2021; 592:756–762 [View Article] [PubMed]
     [Google Scholar]
  128. Rhie A, McCarthy SA, Fedrigo O, Damas J, Formenti G et al. Towards complete and error-free genome assemblies of all vertebrate species. Nature 2021; 592:737–746 [View Article] [PubMed]
     [Google Scholar]
  129. Muller H, Gil J, Drinnenberg IA. The impact of centromeres on spatial genome architecture. Trends Genet 2019; 35:565–578 [View Article] [PubMed]
     [Google Scholar]
  130. Marbouty M, Cournac A, Flot J-F, Marie-Nelly H, Mozziconacci J et al. Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms. eLife 2014; 3:e03318 [View Article] [PubMed]
     [Google Scholar]
  131. Marie-Nelly H, Marbouty M, Cournac A, Liti G, Fischer G et al. Filling annotation gaps in yeast genomes using genome-wide contact maps. Bioinformatics 2014; 30:2105–2113 [View Article] [PubMed]
     [Google Scholar]
  132. Descorps-Declère S, Saguez C, Cournac A, Marbouty M, Rolland T et al. Genome-wide replication landscape of Candida glabrata. BMC Biol 2015; 13:69 [View Article] [PubMed]
     [Google Scholar]
  133. Varoquaux N, Liachko I, Ay F, Burton JN, Shendure J et al. Accurate identification of centromere locations in yeast genomes using Hi-C. Nucleic Acids Res 2015; 43:5331–5339 [View Article] [PubMed]
     [Google Scholar]
  134. Burrack LS, Hutton HF, Matter KJ, Clancey SA, Liachko I et al. Neocentromeres provide chromosome segregation accuracy and centromere clustering to multiple loci along a Candida albicans chromosome. PLoS Genet 2016; 12:e1006317 [View Article] [PubMed]
     [Google Scholar]
  135. Talbert PB, Henikoff S. What makes a centromere?. Exp Cell Res 2020; 389:111895 [View Article] [PubMed]
     [Google Scholar]
  136. Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 2001; 293:1098–1102 [View Article] [PubMed]
     [Google Scholar]
  137. Black BE, Bassett EA. The histone variant CENP-A and centromere specification. Curr Opin Cell Biol 2008; 20:91–100 [View Article] [PubMed]
     [Google Scholar]
  138. Drinnenberg IA, deYoung D, Henikoff S, Malik HS. Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. eLife 2014; 3:e03676 [View Article] [PubMed]
     [Google Scholar]
  139. Cremer T, Cremer M. Chromosome territories. Cold Spring Harb Perspect Biol 2010; 2:a003889 [View Article] [PubMed]
     [Google Scholar]
  140. Szabo Q, Bantignies F, Cavalli G. Principles of genome folding into topologically associating domains. Sci Adv 2019; 5:eaaw1668 [View Article] [PubMed]
     [Google Scholar]
  141. Belton J-M, Lajoie BR, Audibert S, Cantaloube S, Lassadi I et al. The conformation of yeast chromosome III is mating type dependent and controlled by the recombination enhancer. Cell Rep 2015; 13:1855–1867 [View Article] [PubMed]
     [Google Scholar]
  142. Mercy G, Mozziconacci J, Scolari VF, Yang K, Zhao G et al. 3D organization of synthetic and scrambled chromosomes. Science 2017; 355:eaaf4597 [View Article] [PubMed]
     [Google Scholar]
  143. Shao Y, Lu N, Wu Z, Cai C, Wang S et al. Creating a functional single-chromosome yeast. Nature 2018; 560:331–335 [View Article] [PubMed]
     [Google Scholar]
  144. Li M, Fine RD, Dinda M, Bekiranov S, Smith JS. A Sir2-regulated locus control region in the recombination enhancer of Saccharomyces cerevisiae specifies chromosome III structure. PLoS Genet 2019; 15:e1008339 [View Article] [PubMed]
     [Google Scholar]
  145. Hoencamp C, Dudchenko O, Elbatsh AMO, Brahmachari S, Raaijmakers JA et al. 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science 2021; 372:984–989 [View Article] [PubMed]
     [Google Scholar]
  146. IJdo JW, Baldini A, Ward DC, Reeders ST, Wells RA. Origin of human chromosome 2: an ancestral telomere-telomere fusion. Proc Natl Acad Sci U S A 1991; 88:9051–9055 [View Article] [PubMed]
     [Google Scholar]
  147. Cicconardi F, Lewis JJ, Martin SH, Reed RD, Danko CG et al. Chromosome fusion affects genetic diversity and evolutionary turnover of functional loci but consistently depends on chromosome size. Mol Biol Evol 2021; 38:4449–4462 [View Article] [PubMed]
     [Google Scholar]
  148. Luo J, Sun X, Cormack BP, Boeke JD. Karyotype engineering by chromosome fusion leads to reproductive isolation in yeast. Nature 2018; 560:392–396 [View Article] [PubMed]
     [Google Scholar]
  149. Sears ER, Câmara A. A transmissible dicentric chromosome. Genetics 1952; 37:125–135 [View Article] [PubMed]
     [Google Scholar]
  150. Luo MC, Deal KR, Akhunov ED, Akhunova AR, Anderson OD et al. Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae. Proc Natl Acad Sci U S A 2009; 106:15780–15785 [View Article] [PubMed]
     [Google Scholar]
  151. Pobiega S, Marcand S. Dicentric breakage at telomere fusions. Genes Dev 2010; 24:720–733 [View Article] [PubMed]
     [Google Scholar]
  152. Barra V, Fachinetti D. The dark side of centromeres: types, causes and consequences of structural abnormalities implicating centromeric DNA. Nat Commun 2018; 9:4340 [View Article] [PubMed]
     [Google Scholar]
  153. Becker SA, Spreafico R, Kit JL, Brown R, Likhogrud M et al. Phased diploid genome sequence for the fast-growing microalga Picochlorum celeri. Microbiol Resour Announc 2020; 9:e00087–00020 [View Article] [PubMed]
     [Google Scholar]
  154. De Storme N, Mason A. Plant speciation through chromosome instability and ploidy change: Cellular mechanisms, molecular factors and evolutionary relevance. Curr. Plant Biol. 2014; 1:10–33 [View Article]
     [Google Scholar]
  155. Feulner PGD, De-Kayne R. Genome evolution, structural rearrangements and speciation. J Evol Biol 2017; 30:1488–1490 [View Article] [PubMed]
     [Google Scholar]
  156. Rose MD, Novick P, Thomas JH, Botstein D, Fink GR. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 1987; 60:237–243 [View Article] [PubMed]
     [Google Scholar]
  157. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. Multifunctional yeast high-copy-number shuttle vectors. Gene 1992; 110:119–122 [View Article] [PubMed]
     [Google Scholar]
  158. Clarke L, Carbon J. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 1980; 287:504–509 [View Article] [PubMed]
     [Google Scholar]
  159. Murray AW, Szostak JW. Construction of artificial chromosomes in yeast. Nature 1983; 305:189–193 [View Article] [PubMed]
     [Google Scholar]
  160. Ikeno M, Grimes B, Okazaki T, Nakano M, Saitoh K et al. Construction of YAC-based mammalian artificial chromosomes. Nat Biotechnol 1998; 16:431–439 [View Article] [PubMed]
     [Google Scholar]
  161. Karas BJ, Diner RE, Lefebvre SC, McQuaid J, Phillips APR et al. Designer diatom episomes delivered by bacterial conjugation. Nat Commun 2015; 6:6925 [View Article] [PubMed]
     [Google Scholar]
  162. Diner RE, Noddings CM, Lian NC, Kang AK, McQuaid JB et al. Diatom centromeres suggest a mechanism for nuclear DNA acquisition. Proc Natl Acad Sci U S A 2017; 114:E6015–E6024 [View Article] [PubMed]
     [Google Scholar]
  163. Diner RE, Bielinski VA, Dupont CL, Allen AE, Weyman PD. Refinement of the diatom episome maintenance sequence and improvement of conjugation-based DNA delivery methods. Front Bioeng Biotechnol 2016; 4:65 [View Article] [PubMed]
     [Google Scholar]
  164. Jiang L, Lu Y, Zheng L, Li G, Chen L et al. The algal selenoproteomes. BMC Genomics 2020; 21:699 [View Article] [PubMed]
     [Google Scholar]
  165. Serrão VHB, Silva IR, da Silva MTA, Scortecci JF, de Freitas Fernandes A et al. The unique tRNASec and its role in selenocysteine biosynthesis. Amino Acids 2018; 50:1145–1167 [View Article] [PubMed]
     [Google Scholar]
  166. Papp LV, Lu J, Holmgren A, Khanna KK. From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal 2007; 9:775–806 [View Article] [PubMed]
     [Google Scholar]
  167. Turanov AA, Xu X-M, Carlson BA, Yoo M-H, Gladyshev VN et al. Biosynthesis of selenocysteine, the 21st amino acid in the genetic code, and a novel pathway for cysteine biosynthesis. Adv Nutr 2011; 2:122–128 [View Article] [PubMed]
     [Google Scholar]
  168. Novoselov SV, Rao M, Onoshko NV, Zhi H, Kryukov GV et al. Selenoproteins and selenocysteine insertion system in the model plant cell system, Chlamydomonas reinhardtii. EMBO J 2002; 21:3681–3693 [View Article] [PubMed]
     [Google Scholar]
  169. Rayman MP. Selenium and human health. Lancet 2012; 379:1256–1268 [View Article] [PubMed]
     [Google Scholar]
  170. Zoidis E, Seremelis I, Kontopoulos N, Danezis GP. Selenium-dependent antioxidant enzymes: actions and properties of selenoproteins. Antioxidants 2018; 7:66 [View Article] [PubMed]
     [Google Scholar]
  171. Mariotti M, Salinas G, Gabaldón T, Gladyshev VN. Utilization of selenocysteine in early-branching fungal phyla. Nat Microbiol 2019; 4:759–765 [View Article] [PubMed]
     [Google Scholar]
  172. Liang H, Wei T, Xu Y, Li L, Kumar Sahu S et al. Phylogenomics provides new insights into gains and losses of selenoproteins among Archaeplastida. Int J Mol Sci 2019; 20:12 [View Article] [PubMed]
     [Google Scholar]
  173. Lobanov AV, Fomenko DE, Zhang Y, Sengupta A, Hatfield DL et al. Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life. Genome Biol 2007; 8:R198 [View Article] [PubMed]
     [Google Scholar]
  174. Bock C, Krienitz L, Pröschold T. Taxonomic reassessment of the genus Chlorella (Trebouxiophyceae) using molecular signatures (barcodes), including description of seven new species. Fottea 2011; 11:293–312 [View Article]
     [Google Scholar]
  175. Formighieri C, Cazzaniga S, Kuras R, Bassi R. Biogenesis of photosynthetic complexes in the chloroplast of Chlamydomonas reinhardtii requires ARSA1, a homolog of prokaryotic arsenite transporter and eukaryotic TRC40 for guided entry of tail-anchored proteins. Plant J 2013; 73:850–861 [View Article] [PubMed]
     [Google Scholar]
  176. Blaby-Haas CE, Merchant SS. The ins and outs of algal metal transport. Biochim Biophys Acta 2012; 1823:1531–1552 [View Article] [PubMed]
     [Google Scholar]
  177. Marchand J, Heydarizadeh P, Schoefs B, Spetea C. Ion and metabolite transport in the chloroplast of algae: lessons from land plants. Cell Mol Life Sci 2018; 75:2153–2176 [View Article] [PubMed]
     [Google Scholar]
  178. Goswami RK, Agrawal K, Shah MP, Verma P. Bioremediation of heavy metals from wastewater: a current perspective on microalgae-based future. Lett Appl Microbiol 2022; 75:701–717 [View Article] [PubMed]
     [Google Scholar]
  179. Ali H, Khan E, Sajad MA. Phytoremediation of heavy metals--concepts and applications. Chemosphere 2013; 91:869–881 [View Article] [PubMed]
     [Google Scholar]
  180. Almomani F, Bhosale RR. Bio-sorption of toxic metals from industrial wastewater by algae strains Spirulina platensis and Chlorella vulgaris: application of isotherm, kinetic models and process optimization. Sci Total Environ 2021; 755:142654 [View Article] [PubMed]
     [Google Scholar]
  181. Shanab S, Essa A, Shalaby E. Bioremoval capacity of three heavy metals by some microalgae species (Egyptian Isolates). Plant Signal Behav 2012; 7:392–399 [View Article] [PubMed]
     [Google Scholar]
  182. Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S et al. Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 2020; 11:359 [View Article] [PubMed]
     [Google Scholar]
  183. Goswami RK, Agrawal K, Verma P. Phycoremediation of nitrogen and phosphate from wastewater using Picochlorum sp.: a tenable approach. J Basic Microbiol 2022; 62:279–295 [View Article] [PubMed]
     [Google Scholar]
  184. Levina N, Tötemeyer S, Stokes NR, Louis P, Jones MA et al. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 1999; 18:1730–1737 [View Article] [PubMed]
     [Google Scholar]
  185. Kung C, Martinac B, Sukharev S. Mechanosensitive channels in microbes. Annu Rev Microbiol 2010; 64:313–329 [View Article] [PubMed]
     [Google Scholar]
  186. Booth IR, Blount P. The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves. J Bacteriol 2012; 194:4802–4809 [View Article] [PubMed]
     [Google Scholar]
  187. Basu D, Haswell ES. Plant mechanosensitive ion channels: an ocean of possibilities. Curr Opin Plant Biol 2017; 40:43–48 [View Article] [PubMed]
     [Google Scholar]
  188. Deng Z, Maksaev G, Schlegel AM, Zhang J, Rau M et al. Structural mechanism for gating of a eukaryotic mechanosensitive channel of small conductance. Nat Commun 2020; 11:3690 [View Article] [PubMed]
     [Google Scholar]
  189. Owji AP, Zhao Q, Ji C, Kittredge A, Hopiavuori A et al. Structural and functional characterization of the bestrophin-2 anion channel. Nat Struct Mol Biol 2020; 27:382–391 [View Article] [PubMed]
     [Google Scholar]
  190. Tsunenari T, Sun H, Williams J, Cahill H, Smallwood P et al. Structure-function analysis of the bestrophin family of anion channels. J Biol Chem 2003; 278:41114–41125 [View Article] [PubMed]
     [Google Scholar]
  191. Qu Z, Hartzell HC. Bestrophin Cl- channels are highly permeable to HCO3-. Am J Physiol Cell Physiol 2008; 294:C1371–7 [View Article] [PubMed]
     [Google Scholar]
  192. Reinfelder JR. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Ann Rev Mar Sci 2011; 3:291–315 [View Article] [PubMed]
     [Google Scholar]
  193. Mackinder LCM, Chen C, Leib RD, Patena W, Blum SR et al. A spatial interactome reveals the protein organization of the algal CO2-concentrating mechanism. Cell 2017; 171:133–147 [View Article] [PubMed]
     [Google Scholar]
  194. Chi S, Wu S, Yu J, Wang X, Tang X et al. Phylogeny of C4-photosynthesis enzymes based on algal transcriptomic and genomic data supports an archaeal/proteobacterial origin and multiple duplication for most C4-related genes. PLoS One 2014; 9:e110154 [View Article] [PubMed]
     [Google Scholar]
  195. Mukherjee A, Lau CS, Walker CE, Rai AK, Prejean CI et al. Thylakoid localized bestrophin-like proteins are essential for the CO2 concentrating mechanism of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 2019; 116:16915–16920 [View Article] [PubMed]
     [Google Scholar]
  196. Falkowski PG. The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth Res 1994; 39:235–258 [View Article] [PubMed]
     [Google Scholar]
  197. Worden AZ, Nolan JK, Palenik B. Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnol Oceanogr 2004; 49:168–179 [View Article]
     [Google Scholar]
  198. Sheen J. C4 Gene expression. Annu Rev Plant Physiol Plant Mol Biol 1999; 50:187–217 [View Article] [PubMed]
     [Google Scholar]
  199. Matsuoka M, Furbank RT, Fukayama H, Miyao M. Molecular engineering of C4 photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 2001; 52:297–314 [View Article] [PubMed]
     [Google Scholar]
  200. Reiskind JB, Bowes G. The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci U S A 1991; 88:2883–2887 [View Article] [PubMed]
     [Google Scholar]
  201. Xu J, Fan X, Zhang X, Xu D, Mou S et al. Evidence of coexistence of C₃ and C₄ photosynthetic pathways in a green-tide-forming alga, Ulva prolifera. PLoS One 2012; 7:e37438 [View Article] [PubMed]
     [Google Scholar]
  202. Liu D, Ma Q, Valiela I, Anderson DM, Keesing JK et al. Role of C4 carbon fixation in Ulva prolifera, the macroalga responsible for the world’s largest green tides. Commun Biol 2020; 3:494 [View Article] [PubMed]
     [Google Scholar]
  203. Zhang X, Ye N, Liang C, Mou S, Fan X et al. De novo sequencing and analysis of the Ulva linza transcriptome to discover putative mechanisms associated with its successful colonization of coastal ecosystems. BMC Genomics 2012; 13:565 [View Article] [PubMed]
     [Google Scholar]
  204. Xu J, Zhang X, Ye N, Zheng Z, Mou S et al. Activities of principal photosynthetic enzymes in green macroalga Ulva linza: functional implication of C₄ pathway in CO₂ assimilation. Sci China Life Sci 2013; 56:571–580 [View Article] [PubMed]
     [Google Scholar]
  205. Bowes G, Rao SK, Estavillo GM, Reiskind JB. C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct Plant Biol 2002; 29:379–392 [View Article] [PubMed]
     [Google Scholar]
  206. Maberly SC, Madsen TV. Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. Funct Plant Biol 2002; 29:393–405 [View Article] [PubMed]
     [Google Scholar]
  207. Giordano M, Beardall J, Raven JA. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 2005; 56:99–131 [View Article] [PubMed]
     [Google Scholar]
  208. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009; 25:119–120 [View Article] [PubMed]
     [Google Scholar]
  209. Kanehisa M, Sato Y. KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci 2020; 29:28–35 [View Article] [PubMed]
     [Google Scholar]
  210. Kanehisa M, Sato Y, Kawashima M. KEGG mapping tools for uncovering hidden features in biological data. Protein Sci 2022; 31:47–53 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.001223
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Chromosome-scale assembly of the streamlined picoeukaryote Picochlorum sp. SENEW3 genome reveals Rabl-like chromatin structure and potential for C4 photosynthesis
M Gen 10, 001223 (2024); https://doi.org/10.1099/mgen.0.001223
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