Applied Microbiology and Biotechnology

, Volume 102, Issue 7, pp 3049–3058 | Cite as

Two or three domains: a new view of tree of life in the genomics era

Mini-Review

Abstract

The deep phylogenetic topology of tree of life is in the center of a long-time dispute. The Woeseian three-domain tree theory, with the Eukarya evolving as a sister clade to Archaea, competes with the two-domain tree theory (the eocyte tree), with the Eukarya branched within Archaea. Revealed by the ongoing debate over the last three decades, sophisticated and proper phylogenetic methods should necessarily be paid with more emphasis, especially these are focusing on the compositional heterogeneity of sites and lineages, and the heterotachy issue. The newly emerging archaeal lineages with numerous eukaryotic-like features, such as membrane trafficking and cellular compartmentalization, are phylogenetically the closest to eukaryotes currently. These findings highlight the evolutionary history from an ancient archaeon to a more complex archaeon with protoeukaryotic-like features and complex cellular structures, thus providing clues to understand eukaryogenesis process. The increasing repertoire of precise genomic contents provides great advantages on understanding the deep phylogeny of tree of life and ancient evolutionary events on Eukarya branching process.

Keywords

Tree of life Eocyte tree Woeseian tree Asgard superphylum Eukaryotic-like features 

Notes

Acknowledgments

We thank for presentations, critiques, and comments from Prof. Norman R. Pace, Prof. Jared R. Leadbetter, and valuable discussions by the participants in the 2016 MBL microbial diversity summer course. We also thank Prof. William F. Martin for his suggestions on this work.

Author contributions

Z.Z., Y.L., M.L., and J.D.G. conceived the review. Z.Z., Y.L., and M.L. wrote the original manuscript and prepared the tables and figures. M.L. and J.D.G. reviewed and edited the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

References

  1. Abrahão JS, Araújo R, Colson P, La Scola B (2017) The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses. PLoS Genet 13(2):e1006532.  https://doi.org/10.1371/journal.pgen.1006532 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Albani AE, Bengtson S, Canfield DE, Bekker A, Macchiarelli R, Mazurier A, Hammarlund EU, Boulvais P, Dupuy J-J, Fontaine C, Fürsich FT, Gauthier-Lafaye F, Janvier P, Javaux E, Ossa FO, Pierson-Wickmann A-C, Riboulleau A, Sardini P, Vachard D, Whitehouse M, Meunier A (2010) Large colonial organisms with coordinated growth in oxygenated environments 2.1Gyr ago. Nature 466(7302):100–104.  https://doi.org/10.1038/nature09166 CrossRefPubMedGoogle Scholar
  3. Archibald JM (2008) The eocyte hypothesis and the origin of eukaryotic cells. Proc Natl Acad Sci U S A 105(51):20049–20050.  https://doi.org/10.1073/pnas.0811118106 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bapteste E, Brochier C (2004) On the conceptual difficulties in rooting the tree of life. Trends Microbiol 12(1):9–13.  https://doi.org/10.1016/j.tim.2003.11.002 CrossRefPubMedGoogle Scholar
  5. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311(5765):1283–1287.  https://doi.org/10.1126/science.1123061 CrossRefPubMedGoogle Scholar
  6. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM (2008) The archaebacterial origin of eukaryotes. Proc Natl Acad Sci U S A 105(51):20356–20361.  https://doi.org/10.1073/pnas.0810647105 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Da Cunha V, Gaia M, Gadelle D, Nasir A, Forterre P (2017) Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet 13(6):e1006810.  https://doi.org/10.1371/journal.pgen.1006810 CrossRefPubMedPubMedCentralGoogle Scholar
  8. de Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Genet 8(5):395–403.  https://doi.org/10.1038/nrg2071 CrossRefPubMedGoogle Scholar
  9. Degli Esposti M (2016) Late mitochondrial acquisition, really? Genome Biol Evol 8(6):2031–2035.  https://doi.org/10.1093/gbe/evw130 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Eme L, Spang A, Lombard J, Stairs CW, Ettema TJ (2017) Archaea and the origin of eukaryotes. Nat Rev Microbiol 15(12):711–723.  https://doi.org/10.1038/nrmicro.2017.133 CrossRefPubMedGoogle Scholar
  11. Esser C, Ahmadinejad N, Wiegand C, Rotte C, Sebastiani F, Gelius-Dietrich G, Henze K, Kretschmann E, Richly E, Leister D, Bryant D, Steel MA, Lockhart PJ, Penny D, Martin W (2004) A genome phylogeny for mitochondria among α-Proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol 21(9):1643–1660.  https://doi.org/10.1093/molbev/msh160 CrossRefPubMedGoogle Scholar
  12. Ettema TJG (2016) Evolution: mitochondria in the second act. Nature 531(7592):39–40.  https://doi.org/10.1038/nature16876 CrossRefPubMedGoogle Scholar
  13. Ettema TJG, Lindås A-C, Bernander R (2011) An actin-based cytoskeleton in archaea. Mol Microbiol 80(4):1052–1061.  https://doi.org/10.1111/j.1365-2958.2011.07635.x CrossRefPubMedGoogle Scholar
  14. Forterre P (2010) Giant viruses: conflicts in revisiting the virus concept. Intervirology 53(5):362–378.  https://doi.org/10.1159/000312921 CrossRefPubMedGoogle Scholar
  15. Forterre P (2015) The universal tree of life: an update. Front Microbio 6:717.  https://doi.org/10.3389/fmicb.2015.00717 CrossRefGoogle Scholar
  16. Foster PG (2004) Modeling compositional heterogeneity. Syst Biol 53(3):485–495.  https://doi.org/10.1080/10635150490445779 CrossRefPubMedGoogle Scholar
  17. Foster PG, Cox CJ, Embley TM (2009) The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods. Philos Trans R Soc Lond Ser B Biol Sci 364(1527):2197–2207.  https://doi.org/10.1098/rstb.2009.0034 CrossRefGoogle Scholar
  18. Fuerst JA (2005) Intracellular compartmentation in Planctomycetes. Annu Rev Microbiol 59:299–328.  https://doi.org/10.1146/annurev.micro.59.030804.121258 CrossRefPubMedGoogle Scholar
  19. Guy L, Ettema TJ (2011) The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol 19(12):580–587.  https://doi.org/10.1016/j.tim.2011.09.002 CrossRefPubMedGoogle Scholar
  20. He Y, Li M, Perumal V, Feng X, Fang J, Xie J, Sievert SM, Wang F (2016) Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 1(6):16035.  https://doi.org/10.1038/nmicrobiol.2016.35 CrossRefPubMedGoogle Scholar
  21. Heimerl T, Flechsler J, Pickl C, Heinz V, Salecker B, Zweck J, Wanner G, Geimer S, Samson RY, Bell SD, Huber H, Wirth R, Wurch L, Podar M, Rachel R (2017) A complex endomembrane system in the archaeon Ignicoccus hospitalis tapped by Nanoarchaeum equitans. Front Microbiol 8(1072)  https://doi.org/10.3389/fmicb.2017.01072
  22. Heinz E, Domman D (2017) Reshaping the tree of life. Nat Rev Microbiol 15(6):322–322.  https://doi.org/10.1038/nrmicro.2017.51 CrossRefPubMedGoogle Scholar
  23. Hong Y, Cao H, Li M, Gu J-D (2014) Anammoxosome in anaerobic ammonium-oxidizing bacteria—was it originated from endosymbiosis? Am J Curr Microbiol 2:18–40Google Scholar
  24. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K (2016) A new view of the tree of life. Nat Microbiol 1:16048.  https://doi.org/10.1038/nmicrobiol.2016.48 CrossRefPubMedGoogle Scholar
  25. Küper U, Meyer C, Müller V, Rachel R, Huber H (2010) Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic Archaeon Ignicoccus hospitalis. Proc Natl Acad Sci U S A 107(7):3152–3156.  https://doi.org/10.1073/pnas.0911711107 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Katoh K, Kuma K-i, Miyata T (2001) Genetic algorithm-based maximum-likelihood analysis for molecular phylogeny. J Mol Evol 53(4):477–484.  https://doi.org/10.1007/s002390010238 CrossRefPubMedGoogle Scholar
  27. Kelly S, Wickstead B, Gull K (2011) Archaeal phylogenomics provides evidence in support of a methanogenic origin of the archaea and a thaumarchaeal origin for the eukaryotes. Proc R Soc Lond B Biol Sci 278(1708):1009–1018.  https://doi.org/10.1098/rspb.2010.1427 CrossRefGoogle Scholar
  28. Klinger CM, Spang A, Dacks JB, Ettema TJG (2016) Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol Biol Evol 33(6):1528–1541.  https://doi.org/10.1093/molbev/msw034 CrossRefPubMedGoogle Scholar
  29. Kolaczkowski B, Thornton JW (2004) Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431(7011):980–984.  https://doi.org/10.1038/nature02917 CrossRefPubMedGoogle Scholar
  30. Koonin EV, Yutin N (2010) Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses. Intervirology 53(5):284–292.  https://doi.org/10.1159/000312913 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kubatko LS, Degnan JH (2007) Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 56(1):17–24.  https://doi.org/10.1080/10635150601146041 CrossRefPubMedGoogle Scholar
  32. López-García P, Moreira D (2015) Open questions on the origin of eukaryotes. Trends Ecol Evol 30(11):697–708.  https://doi.org/10.1016/j.tree.2015.09.005 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lake JA (1988) Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature 331(6152):184–186.  https://doi.org/10.1038/331184a0 CrossRefPubMedGoogle Scholar
  34. Lake JA (1990) Archaebacterial or eocyte tree? Nature 343(6257):418–419.  https://doi.org/10.1038/343418b0 CrossRefGoogle Scholar
  35. Lake JA (1991) The order of sequence alignment can bias the selection of tree topology. Mol Biol Evol 8(3):378–385PubMedGoogle Scholar
  36. Lake JA (1994) Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances. Proc Natl Acad Sci U S A 91(4):1455–1459.  https://doi.org/10.1073/pnas.91.4.1455 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lake JA (2015) Eukaryotic origins. Philos Trans R Soc Lond Ser B Biol Sci 370(1678):20140321.  https://doi.org/10.1098/rstb.2014.0321 CrossRefGoogle Scholar
  38. Lake JA, Henderson E, Oakes M, Clark MW (1984) Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc Natl Acad Sci U S A 81(12):3786–3790CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lang BF, Gray MW, Burger G (1999) Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet 33(1):351–397.  https://doi.org/10.1146/annurev.genet.33.1.351 CrossRefPubMedGoogle Scholar
  40. Lester L, Meade A, Pagel M (2006) The slow road to the eukaryotic genome. BioEssays 28(1):57–64.  https://doi.org/10.1002/bies.20344 CrossRefPubMedGoogle Scholar
  41. Li M, Baker BJ, Anantharaman K, Jain S, Breier JA, Dick GJ (2015) Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea. Nat Commun 6:8933.  https://doi.org/10.1038/ncomms9933 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lindås A-C, Karlsson EA, Lindgren MT, Ettema TJG, Bernander R (2008) A unique cell division machinery in the archaea. Proc Natl Acad Sci U S A 105(48):18942–18946.  https://doi.org/10.1073/pnas.0809467105 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Liu Y, Zhou Z, Pan J, Baker B, Gu J-D, Li M (2018) Comparative genomic inference suggests mixotrophic lifestyle for Thorarchaeota. ISME J.  https://doi.org/10.1038/s41396-018-0060-x
  44. Lopez P, Casane D, Philippe H (2002) Heterotachy, an important process of protein evolution. Mol Biol Evol 19(1):1–7.  https://doi.org/10.1093/oxfordjournals.molbev.a003973 CrossRefPubMedGoogle Scholar
  45. Lopez P, Forterre P, Philippe H (1999) The root of the tree of life in the light of the covarion model. J Mol Evol 49(4):496–508.  https://doi.org/10.1007/pl00006572 CrossRefPubMedGoogle Scholar
  46. Makarova KS, Yutin N, Bell SD, Koonin EV (2010) Evolution of diverse cell division and vesicle formation systems in Archaea. Nat Rev Microbiol 8(10):731–741.  https://doi.org/10.1038/nrmicro2406 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Martin W, Muller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392(6671):37–41.  https://doi.org/10.1038/32096 CrossRefPubMedGoogle Scholar
  48. Martin WF, Weiss MC, Neukirchen S, Nelson-Sathi S, Sousa FL (2016) Physiology, phylogeny, and LUCA. Microbial Cell 3(12):451–456.  https://doi.org/10.15698/mic2016.12.545 CrossRefGoogle Scholar
  49. Meng J, Xu J, Qin D, He Y, Xiao X, Wang F (2014) Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J 8(3):650–659.  https://doi.org/10.1038/ismej.2013.174 CrossRefPubMedGoogle Scholar
  50. Nasir A, Kim KM, Da Cunha V, Caetano-Anollés G (2016) Arguments reinforcing the three-domain view of diversified cellular life. Archaea 2016:11.  https://doi.org/10.1155/2016/1851865 CrossRefGoogle Scholar
  51. Pace NR (2016) Comments from norm pace on the recent hug et al. “eocyte” phylogenetic tree. In: pace NR (ed). Comments ednGoogle Scholar
  52. Pace NR, Sapp J, Goldenfeld N (2012) Phylogeny and beyond: scientific, historical, and conceptual significance of the first tree of life. Proc Natl Acad Sci U S A 109(4):1011–1018.  https://doi.org/10.1073/pnas.1109716109 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Philippe H, Forterre P (1999) The rooting of the universal tree of life is not reliable. J Mol Evol 49(4):509–523.  https://doi.org/10.1007/pl00006573 CrossRefPubMedGoogle Scholar
  54. Pittis AA, Gabaldón T (2016) Late acquisition of mitochondria by a host with chimeric prokaryotic ancestry. Nature 531(7592):101–104.  https://doi.org/10.1038/nature16941 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Poole AM, Neumann N (2011) Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis. Res Microbiol 162(1):71–76.  https://doi.org/10.1016/j.resmic.2010.10.002 CrossRefPubMedGoogle Scholar
  56. Raymann K, Brochier-Armanet C, Gribaldo S (2015) The two-domain tree of life is linked to a new root for the Archaea. Proc Natl Acad Sci U S A 112(21):6670–6675.  https://doi.org/10.1073/pnas.1420858112 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rivera MC, Jain R, Moore JE, Lake JA (1998) Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci U S A 95(11):6239–6244CrossRefPubMedPubMedCentralGoogle Scholar
  58. Rochette NC, Brochier-Armanet C, Gouy M (2014) Phylogenomic test of the hypotheses for the evolutionary origin of eukaryotes. Mol Biol Evol 31:832–845.  https://doi.org/10.1093/molbev/mst272 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Roger AJ, Muñoz-Gómez SA, Kamikawa R (2017) The origin and diversification of mitochondria. Curr Biol 27(21):R1177–R1192.  https://doi.org/10.1016/j.cub.2017.09.015 CrossRefPubMedGoogle Scholar
  60. Schulz F, Yutin N, Ivanova NN, Ortega DR, Lee TK, Vierheilig J, Daims H, Horn M, Wagner M, Jensen GJ, Kyrpides NC, Koonin EV, Woyke T (2017) Giant viruses with an expanded complement of translation system components. Science 356(6333):82–85.  https://doi.org/10.1126/science.aal4657 CrossRefPubMedGoogle Scholar
  61. Seitz KW, Lazar CS, Hinrichs K-U, Teske AP, Baker BJ (2016) Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J 10(7):1696–1705.  https://doi.org/10.1038/ismej.2015.233 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sidow A, Wilson AC (1990) Compositional statistics: an improvement of evolutionary parsimony and its application to deep branches in the tree of life. J Mol Evol 31(1):51–68.  https://doi.org/10.1007/bf02101792 CrossRefPubMedGoogle Scholar
  63. Sousa FL, Neukirchen S, Allen JF, Lane N, Martin WF (2016) Lokiarchaeon is hydrogen dependent. Nat Microbiol 1:16034.  https://doi.org/10.1038/nmicrobiol.2016.34 CrossRefPubMedGoogle Scholar
  64. Spang A, Eme L, Saw JH, Caceres EF, Zaremba-Niedzwiedzka K, Lombard J, Guy L, Ettema TJG (2017) Asgard archaea are the closest archaeal relatives of eukaryotes. Plos Genet (in the press)Google Scholar
  65. Spang A, Saw JH, Jorgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJG (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521(7551):173–179.  https://doi.org/10.1038/nature14447 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Tabak H, Hoepfner D, Vd Zand A, Geuze H, Braakman I, Huynen M (2006) Formation of peroxisomes: present and past. Biochim Biophys Acta 1763(12):1647–1654CrossRefPubMedGoogle Scholar
  67. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135CrossRefPubMedGoogle Scholar
  68. Tourasse NJ, Gouy M (1999) Accounting for evolutionary rate variation among sequence sites consistently changes universal phylogenies deduced from rRNA and protein-coding genes. Mol Phylogen Evol 13(1):159–168.  https://doi.org/10.1006/mpev.1999.0675 CrossRefGoogle Scholar
  69. van der Gulik PTS, Hoff WD, Speijer D (2017) In defence of the three-domains of life paradigm. BMC Evol Biol 17(1):218.  https://doi.org/10.1186/s12862-017-1059-z CrossRefPubMedPubMedCentralGoogle Scholar
  70. Vanwonterghem I, Evans PN, Parks DH, Jensen PD, Woodcroft BJ, Hugenholtz P, Tyson GW (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol 1:16170CrossRefPubMedGoogle Scholar
  71. Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin WF (2016) The physiology and habitat of the last universal common ancestor. Nat Microbiol 1:16116.  https://doi.org/10.1038/nmicrobiol.2016.116 CrossRefPubMedGoogle Scholar
  72. Williams TA, Embley TM (2014) Archaeal “dark matter” and the origin of eukaryotes. Genome Biol Evol 6(3):474–481.  https://doi.org/10.1093/gbe/evu031 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504(7479):231–236.  https://doi.org/10.1038/nature12779 CrossRefPubMedGoogle Scholar
  74. Williams TA, Foster PG, Nye TMW, Cox CJ, Embley TM (2012) A congruent phylogenomic signal places eukaryotes within the Archaea. Proc R Soc Lond B Biol Sci 279(1749):4870–4879.  https://doi.org/10.1098/rspb.2012.1795 CrossRefGoogle Scholar
  75. Williams TA, Szöllősi GJ, Spang A, Foster PG, Heaps SE, Boussau B, Ettema TJG, Embley TM (2017) Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proc Natl Acad Sci U S A 114(23):E4602–E4611.  https://doi.org/10.1073/pnas.1618463114 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Woese CR (1987) Bacterial evolution. Microbiol Rev 51(2):221–271PubMedPubMedCentralGoogle Scholar
  77. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 74(11):5088–5090.  https://doi.org/10.1073/pnas.74.11.5088 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87(12):4576–4579CrossRefPubMedPubMedCentralGoogle Scholar
  79. Yang Z, Roberts D (1995) On the use of nucleic acid sequences to infer early branchings in the tree of life. Mol Biol Evol 12(3):451–458PubMedGoogle Scholar
  80. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L, Vancaester E, Seitz KW, Anantharaman K, Starnawski P, Kjeldsen KU, Stott MB, Nunoura T, Banfield JF, Schramm A, Baker BJ, Spang A, Ettema TJG (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541(7637):353–358.  https://doi.org/10.1038/nature21031 CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Institute for Advanced StudyShenzhen UniversityShenzhenPeople’s Republic of China
  2. 2.Laboratory of Environmental Microbiology and Toxicology, School of Biological SciencesThe University of Hong KongHong KongPeople’s Republic of China
  3. 3.Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Optoelectronic EngineeringShenzhen UniversityShenzhenPeople’s Republic of China

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