Advertisement

Protoplasma

pp 1–14 | Cite as

Identification, classification, and evolution of putative xylosyltransferases from algae

  • Wentao Han
  • Xiao Fan
  • Linhong Teng
  • Michelle Joyce Slade Kaczurowski
  • Xiaowen Zhang
  • Dong Xu
  • Yanbin Yin
  • Naihao YeEmail author
Original Article
  • 77 Downloads

Abstract

Xylosyltransferases (XylTs) play key roles in the biosynthesis of many different polysaccharides. These enzymes transfer d-xylose from UDP-xylose to substrate acceptors. In this study, we identified 30 XylTs from primary endosymbionts (green algae, red algae, and glaucophytes) and secondary or higher endosymbionts (brown algae, diatoms, Eustigmatophyceae, Pelagophyceae, and Cryptophyta). We performed comparative phylogenetic studies on key XylT subfamilies, and investigated the functional divergence of genes using RNA-Seq. Of the 30 XylTs, one β-1,4-XylT IRX14-related, one β-1,4 XylT IRX10L-related, and one xyloglucan 6-XylT 1-related gene were identified in the Charophyta, showing strong similarities to their land plant descendants. This implied the ancient occurrence of xylan and xyloglucan biosynthetic machineries in Charophyta. The other 27 XylTs were identified as UDP-d-xylose: l-fucose-α-1,3-d-XylT (FucXylT) type that specifically transferred d-xylose to fucose. We propose that FucXylTs originated from the last eukaryotic common ancestor, rather than being plant specific, because they are also distributed in Choanoflagellatea and Echinodermata. Considering the evidence from many aspects, we hypothesize that the FucXylTs likely participated in fucoidan biosynthesis in brown algae. We provide the first insights into the evolutionary history and functional divergence of FucXylT in algal biology.

Keywords

Xylosyltransferase evolution Algal polysaccharides Functional divergence 

Notes

Author contributions

N.Y. planned and designed the research. W.H., X.F., and L. T analyzed and interpreted the data for the work. W.H wrote the manuscript. M. J. S. K., X.D., X.Z., and Y. Y. revised it critically for important intellectual content.

Funding information

This work was supported by the national key research and development program of China (2018YFD0900703, 2016YFC1402102, 2018YFD0901503-8), Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (NO. 2018SDKJ0406-3); Financial Fund of the Ministry of Agriculture and Rural Affairs, P. R. of China (NFZX2018). Projects of International Exchange and Cooperation in Agriculture, Ministry of Agriculture and Rural Affairs of China-Science, Technology and Innovation Cooperation in Aquaculture with Tropical Countries along the Belt and Road; Shandong key Research and Development Plan (2018GHY115010); National Natural Science Foundation of China (41676145); China Agriculture Research System (CARS-50); Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (20603022016001, 20603022019006); Taishan Scholars Funding of Shandong Province; Talent Projects of Distinguished Scientific Scholars in Agriculture.

Supplementary material

709_2019_1358_MOESM1_ESM.fasta (19 kb)
Supporting file S1 Sequence data of the 30 hits in target genomes (FASTA 18 kb)
709_2019_1358_MOESM2_ESM.xlsx (23 kb)
Supporting table S1 The numbers of xylosyltransferase subfamily members found in 25 target genomes, including Glaucophyta, Cryptophyta, red algae, green algae, photosynthetic stramenopiles and non-photosynthetic oomycetes. The color indicates the count difference. The 12 xylosyltransferase’ hidden Markov models were downloaded from PANTHER (http://www.pantherdb.org). *Each subfamily belongs to the glycosyltransferase family. ** Only target proteins were counted. (XLSX 23 kb)
709_2019_1358_MOESM3_ESM.xlsx (39 kb)
Supporting table S2 List of sequences used for phylogenetic analyses and their corresponding accession numbers. (XLSX 38 kb)
709_2019_1358_MOESM4_ESM.jpg (3.1 mb)
Supporting figure s1 Phylogeny of the xylosyltransferase domains of 225 proteins. The multiple sequence alignment of the xylosyltransferase protein domains was performed using Clustal Omega (http://www.ebi.ac.uk/Tools/msa/clustalo/). The phylogeny was constructed using the MEGA version 7.0 program (Kumar et al. 2016). Different subfamilies and GT families are represented by different colors. Black asterisks (*) denote proteins in our target genomes. (JPG 3218 kb)
709_2019_1358_MOESM5_ESM.jpg (526 kb)
Supporting figure S2 Phylogeny of the full-length IRX10L proteins. (JPG 525 kb)
709_2019_1358_MOESM6_ESM.jpg (557 kb)
Supporting figure S3 Phylogeny of the full-length IRX14 proteins. (JPG 557 kb)
709_2019_1358_MOESM7_ESM.jpg (641 kb)
Supporting figure S4 Phylogeny of the full-length XXT proteins. (JPG 640 kb)
709_2019_1358_MOESM8_ESM.jpg (1.3 mb)
Supporting figure S5 Phylogeny of the full-length FucXylT proteins. (JPG 1308 kb)
709_2019_1358_MOESM9_ESM.jpg (345 kb)
Supporting figure S6 Sequence identity and similarity levels among 11 FucXylT proteins. (JPG 345 kb)

References

  1. Atmodjo MA, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64:747–779CrossRefGoogle Scholar
  2. Becker DJ, Lowe JB (2003) Fucose: biosynthesis and biological function in mammals. Glycobiology 13:41RCrossRefGoogle Scholar
  3. Berteau O, Mulloy B (2003) Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 13:29RCrossRefGoogle Scholar
  4. Bilan MI, Shashkov AS, Usov AI (2014) Structure of a sulfated xylofucan from the brown alga Punctaria plantaginea. Carbohydr Res 393:1–8CrossRefGoogle Scholar
  5. Breton C, Snajdrová L, Jeanneau C, Koca J, Imberty A (2006) Structures and mechanisms of glycosyltransferases. Glycobiology 16:29RCrossRefGoogle Scholar
  6. Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295CrossRefGoogle Scholar
  7. Brown DM, Zhang Z, Stephens E, Dupree P, Turner SR (2009) Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J 57:732–746CrossRefGoogle Scholar
  8. Burki F, Flegontov P, Oborník M, Cihlár J, Pain A, Lukes J, Keeling PJ (2012) Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genome Biol Evol 4:626–635CrossRefGoogle Scholar
  9. Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, Raikhel NV, Keegstra K (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519–1537CrossRefGoogle Scholar
  10. Chiniquy D et al (2012) XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc Natl Acad Sci U S A 109:17117–17122CrossRefGoogle Scholar
  11. Chou YH, Pogorelko G, Zabotina OA (2012) Xyloglucan xylosyltransferases XXT1, XXT2, and XXT5 and the glucan synthase CSLC4 form Golgi-localized multiprotein complexes. Plant Physiol 159:1355–1366CrossRefGoogle Scholar
  12. Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury JM, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collén J, Corre E, da Silva C, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, Gachon CMM, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Küpper FC, Lang D, le Bail A, Leblanc C, Lerouge P, Lohr M, Lopez PJ, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli CA, Nelson DR, Nyvall-Collén P, Peters AF, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing SA, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder DC, Ségurens B, Strittmatter M, Tonon T, Tregear JW, Valentin K, von Dassow P, Yamagishi T, van de Peer Y, Wincker P (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621CrossRefGoogle Scholar
  13. Coutinho PM, Deleury E, Davies GJ, Henrissat B (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328:307–317CrossRefGoogle Scholar
  14. Cunha L, Grenha A (2016) Sulfated seaweed polysaccharides as multifunctional materials in drug delivery applications. Marine Drugs:14Google Scholar
  15. Deniaud-Bouët E, Hardouin K, Potin P, Kloareg B, Hervé C (2017) A review about brown algal cell walls and fucose-containing sulfated polysaccharides: cell wall context, biomedical properties and key research challenges. Carbohydr Polym 175:395–408CrossRefGoogle Scholar
  16. Ebringerová A, Heinze T (2000) Xylan and xylan derivatives – biopolymers with valuable properties, 1. Naturally occurring xylans structures, isolation procedures and properties. Macromol Rapid Commun 21:542–556CrossRefGoogle Scholar
  17. Eddy SR (1998) Profile hidden Markov models. Bioinformatics (Oxford, England) 14:755–763CrossRefGoogle Scholar
  18. Egelund J et al (2006) Arabidopsis thaliana RGXT1 and RGXT2 encode Golgi-localized (1,3)-alpha-D-xylosyltransferases involved in the synthesis of pectic rhamnogalacturonan-II. Plant Cell 18:2593CrossRefGoogle Scholar
  19. Egelund J, Damager I, Faber K, Olsen CE, Ulvskov P, Petersen BL (2008) Functional characterisation of a putative rhamnogalacturonan II specific xylosyltransferase. Febs Letters 582:3217–3222CrossRefGoogle Scholar
  20. Evans LV, Simpson M, Callow ME (1973) Sulphated polysaccharide synthesis in brown algae. Planta 110:237–252CrossRefGoogle Scholar
  21. Faik A, Price NJ, Raikhel NV, Keegstra K (2002) An Arabidopsis gene encoding an α-xylosyltransferase involved in xyloglucan biosynthesis. Proc Natl Acad Sci 99:7797–7802CrossRefGoogle Scholar
  22. Fangel JU, Petersen BL, Jensen NB, Willats WGT, Bacic A, Egelund J (2011) A putative Arabidopsis thaliana glycosyltransferase, At4g01220, which is closely related to three plant cell wall-specific xylosyltransferases, is differentially expressed spatially and temporally. Plant J 180:470–479Google Scholar
  23. Götting C, Kuhn J, Zahn R, Brinkmann T, Kleesiek K (2000) Molecular cloning and expression of human UDP-d-Xylose:proteoglycan core protein beta-d-xylosyltransferase and its first isoform XT-II. J Mol Biol 304:517–528CrossRefGoogle Scholar
  24. Hori K et al (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:3978CrossRefGoogle Scholar
  25. Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297CrossRefGoogle Scholar
  26. Ikegaya H, Hayashi T, Kaku T, Iwata K, Sonobe S, Shimmen T (2008) Presence of xyloglucan-like polysaccharide in Spirogyra and possible involvement in cell–cell attachment. Phycol Res 56:216–222CrossRefGoogle Scholar
  27. Jensen JK, Scheller HV (2008) Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis. Plant Cell 20:1289–1302CrossRefGoogle Scholar
  28. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240CrossRefGoogle Scholar
  29. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858CrossRefGoogle Scholar
  30. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870CrossRefGoogle Scholar
  31. Larsen PB et al (2009) Assay and heterologous expression inPichia pastorisof plant cell wall type-II membrane anchored glycosyltransferases. Glycoconj J 26:1235–1246CrossRefGoogle Scholar
  32. Lee C, Ye ZH (2010) Focus issue on plant cell walls: the Arabidopsis Family GT43 glycosyltransferases form two functionally nonredundant groups essential for the elongation of glucuronoxylan backbone. Plant Physiol 153:526–541CrossRefGoogle Scholar
  33. Lee C, O'Neill MA, Tsumuraya Y, Darvill AG, Ye ZH (2007) The irregular xylem9 mutant is deficient in xylan xylosyltransferase activity. Plant Cell Physiol 48:1624–1634CrossRefGoogle Scholar
  34. Lei W, Jing S, Su X, Yu Q, Yu Q, Peng Z (2016) A review about the development of fucoidan in antitumor activity: progress and challenges. Carbohydr Polym 154:96–111CrossRefGoogle Scholar
  35. Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245CrossRefGoogle Scholar
  36. Liu XL, Liu L, Niu QK, Xia C, Yang KZ, Li R, Chen LQ, Zhang XQ, Zhou Y, Ye D (2011) MALE GAMETOPHYTE DEFECTIVE 4 encodes a rhamnogalacturonan II xylosyltransferase and is important for growth of pollen tubes and roots in Arabidopsis. Plant J 65:647–660CrossRefGoogle Scholar
  37. Lombard V, Golaconda HR, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490CrossRefGoogle Scholar
  38. Matsunaga T, Ishii T, Matsumoto S, Higuchi M, Darvill A, Albersheim P, O’Neill MA (2004) Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 134:339–351CrossRefGoogle Scholar
  39. Mi H, Muruganujan A, Casagrande JT, Thomas PD (2013) Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8:1551–1566CrossRefGoogle Scholar
  40. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010a) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol 188:82–97CrossRefGoogle Scholar
  41. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010b) Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol 188:67–81CrossRefGoogle Scholar
  42. Mikkelsen MD, Harholt J, Ulvskov P, Johansen IE, Fangel JU, Doblin MS, Bacic A, Willats WGT (2014) Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae. Ann Bot 114:1217–1236CrossRefGoogle Scholar
  43. Moreira D, Le GH, Philippe H (2000) The origin of red algae and the evolution of chloroplasts. Nature 405:69CrossRefGoogle Scholar
  44. Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726CrossRefGoogle Scholar
  45. Müller S et al (2005) Human xylosyltransferase I: functional and biochemical characterization of cysteine residues required for enzymic activity. Biochem J 386:227–236CrossRefGoogle Scholar
  46. Munns CF, Fahiminiya S, Poudel N, Munteanu MC, Majewski J, Sillence DO, Metcalf JP, Biggin A, Glorieux F, Fassier F, Rauch F, Hinsdale ME (2015) Homozygosity for frameshift mutations in XYLT2 result in a spondylo-ocular syndrome with bone fragility, cataracts, and hearing defects. Am J Hum Genet 96:971–978CrossRefGoogle Scholar
  47. Niklas KJ (2004) The cell walls that bind the tree of life. BioScience 54:831–841CrossRefGoogle Scholar
  48. Nishitsuji K et al (2016) A draft genome of the brown alga, Cladosiphon okamuranus, S-strain: a platform for future studies of ‘mozuku’ biology. DNA Res 23:dsw039CrossRefGoogle Scholar
  49. Pauly M, Keegstra K (2016) Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. Annu Rev Plant Biol 67:235CrossRefGoogle Scholar
  50. Popper ZA, Tuohy MG (2010) Beyond the green: understanding the evolutionary puzzle of plant and algal cell walls. Plant Physiol 153:373–383CrossRefGoogle Scholar
  51. Ren Y, Hansen SF, Ebert B, Lau J, Scheller HV (2014) Site-directed mutagenesis of IRX9, IRX9L and IRX14 proteins involved in xylan biosynthesis: glycosyltransferase activity is not required for IRX9 function in Arabidopsis. PLoS One, 9,8(2014-8-13) 9:e105014CrossRefGoogle Scholar
  52. Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:320–324CrossRefGoogle Scholar
  53. Sethi MK et al (2009) Identification of glycosyltransferase 8 family members as xylosyltransferases acting on O-glucosylated notch EGF repeats. J Biol Chem.  https://doi.org/10.1074/jbc.C109.065409
  54. Sethi MK et al (2012) Molecular cloning of a xylosyltransferase that transfers the second xylose to O-glucosylated epidermal growth factor repeats of notch. J Biol Chem 287:2739–2748CrossRefGoogle Scholar
  55. Sievers F et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539CrossRefGoogle Scholar
  56. Smith J, Yang Y, Levy S, Adelusi OO, Hahn MG, O’Neill MA, Barpeled M (2016) Functional characterization of UDP-apiose synthases from bryophytes and green algae provides insight into the appearance of apiose-containing glycans during plant evolution. J Biol Chem:291Google Scholar
  57. Sørensen I, Domozych D, Willats WG (2010) How have plant cell walls evolved. Plant Physiol 153:366CrossRefGoogle Scholar
  58. Stoolmiller AC, Horwitz AL, Dorfman A (1972) Biosynthesis of the chondroitin sulfate proteoglycan. Purification and properties of xylosyltransferase. J Biol Chem 247:3525–3532Google Scholar
  59. Taujale R, Yin Y (2015) Glycosyltransferase family 43 is also found in early eukaryotes and has three subfamilies in Charophycean green algae. PLoS One 10:e0128409CrossRefGoogle Scholar
  60. Teng L, Han W, Fan X, Xu D, Zhang X, Dittami SM, Ye N (2017) Evolution and expansion of the prokaryote-like lipoxygenase family in the brown alga Saccharina japonica. Front Plant Sci 8:2018.  https://doi.org/10.3389/fpls.2017.02018 CrossRefGoogle Scholar
  61. Turner JE, Mok DW, Mok MC, Shaw G (1987) Isolation and partial purification of an enzyme catalyzing the formation of O-xylosylzeatin in Phaseolus vulgaris embryos. Proc Natl Acad Sci U S A 84:3714–3717CrossRefGoogle Scholar
  62. Ulvskov P (2010) Glycosyltransferases of the GT77 Family. Annu Plant Rev 41:305–320Google Scholar
  63. Ulvskov P, Paiva DS, Domozych D, Harholt J (2013) Classification, naming and evolutionary history of glycosyltransferases from sequenced green and red algal genomes. Plos One 8:131–132CrossRefGoogle Scholar
  64. Vishchuk OS, Ermakova SP, Zvyagintseva TN (2011) Sulfated polysaccharides from brown seaweeds Saccharina japonica and Undaria pinnatifida: isolation, structural characteristics, and antitumor activity. Carbohydr Res 346:2769–2776CrossRefGoogle Scholar
  65. Vishchuk OS, Tarbeeva DV, Ermakova SP, Zvyagintseva TN (2012) Structural characteristics and biological activity of Fucoidans from the brown algae Alaria sp. and Saccharina japonica of different reproductive status. Chem Biodivers 9:817CrossRefGoogle Scholar
  66. Wang XY, Tang Q, Zhao X, Jia C, Yang X, He G, Wu A, Kong Y, Hu R, Zhou G (2016) Functional conservation and divergence of Miscanthus lutarioriparius GT43 gene family in xylan biosynthesis. BMC Plant Biol 16:102CrossRefGoogle Scholar
  67. Wiggins CA, Munro S (1998) Activity of the yeast MNN1 α-1, 3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc Natl Acad Sci 95:7945–7950CrossRefGoogle Scholar
  68. Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B (2011) Origin of land plants: do conjugating green algae hold the key. BMC Evol Biol 11:104CrossRefGoogle Scholar
  69. Wu AM et al (2008) The Arabidopsis IRX10 and IRX10-LIKE glycosyltransferases are critical for glucuronoxylan biosynthesis during secondary cell wall formation. Plant J 57:718CrossRefGoogle Scholar
  70. Wu A-M, Hörnblad E, Voxeur A, Gerber L, Rihouey C, Lerouge P, Marchant A (2010) Analysis of the Arabidopsis IRX9/IRX9-L and IRX14/IRX14-L pairs of glycosyltransferase genes reveals critical contributions to biosynthesis of the hemicellulose glucuronoxylan. Plant Physiol 153:542–554CrossRefGoogle Scholar
  71. Ye N et al (2015) Saccharina genomes provide novel insight into kelp biology. Nat Commun 6:6986CrossRefGoogle Scholar
  72. Yin Y, Chen H, Hahn MG, Mohnen D, Xu Y (2010) Evolution and function of the plant cell wall synthesis-related glycosyltransferase family 8. Plant Physiol 153:1729–1746CrossRefGoogle Scholar
  73. Yin YB, Mao XZ, Yang JC, Xin C, Mao FL, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:445–451CrossRefGoogle Scholar
  74. Zeng W, Lampugnani ER, Picard KL, Song L, Wu AM, Farion IM, Zhao J, Ford K, Doblin MS, Bacic A (2016) Asparagus IRX9, IRX10, and IRX14A are components of an active xylan backbone synthase complex that forms in the Golgi apparatus. Plant Physiol 171:93–109CrossRefGoogle Scholar
  75. Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Wentao Han
    • 1
    • 2
    • 3
  • Xiao Fan
    • 1
  • Linhong Teng
    • 1
    • 4
  • Michelle Joyce Slade Kaczurowski
    • 5
  • Xiaowen Zhang
    • 1
  • Dong Xu
    • 1
  • Yanbin Yin
    • 6
  • Naihao Ye
    • 1
    • 3
    Email author
  1. 1.Yellow Sea Fisheries Research InstituteChinese Academy of Fishery SciencesQingdaoChina
  2. 2.Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of EducationShanghai Ocean UniversityShanghaiChina
  3. 3.Function Laboratory for Marine Fisheries Science and Food Production Processes,Qingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  4. 4.College of Life ScienceDezhou UniversityDezhouChina
  5. 5.Biological SciencesFlinders UniversityAdelaideAustralia
  6. 6.Department of Food Science and TechnologyUniversity of Nebraska—LincolnLincolnUSA

Personalised recommendations