Skip to main content
Log in

The ice-binding proteins of a snow alga, Chloromonas brevispina: probable acquisition by horizontal gene transfer

Extremophiles Aims and scope Submit manuscript

Abstract

All ice-and snow-related unicellular algae examined so far secrete ice-binding proteins (IBPs) to mitigate freezing damage. Two types of IBP have been identified in chlorophytes. Type 1 IBPs are members of a large family of proteins that share a large domain of unknown function (DUF3494). Previous studies have suggested that the type 1 algal IBP genes were acquired by horizontal gene transfer. To test this hypothesis I sequenced the IBP genes of a snow alga, Chloromonas brevispina. The IBPs were identified by ice affinity purification, de novo sequencing of a tryptic peptide and large-scale sequencing of the transcriptome and genome. C. brevispina has genes for over 20 IBP isoforms, which strongly indicates their importance. The IBPs are all of type 1 and match fungal and bacterial proteins more closely than they match known algal IBPs, providing further evidence that the genes were acquired by horizontal transfer. Modeling of the 3D structures of the IBPs based on the known structure of a homologous protein suggests that the ice-binding site has characteristics that are shared by all DUF3494 proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Achberger AM, Brox TI, Skidmore ML, Christner BC (2011) Expression and partial characterization of an ice-binding protein from a bacterium isolated at a depth of 3,519 m in the Vostok Ice Core. Antarctica. Front Microbiol 2:255. doi:10.3389/fmicb.00255(2011)

    Google Scholar 

  • Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22(2):195–201. doi:10.1093/bioinformatics/bti770

    Article  PubMed  CAS  Google Scholar 

  • Becker B, Hoef-Emden K, Melkonian M (2008) Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol Biol 8:203. doi:10.1186/1471-2148-8-203

    Article  PubMed  PubMed Central  Google Scholar 

  • Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: signalP 3.0. J Mol Biol 340(4):783–795. doi:10.1016/j.jmb.2004.05.028)

    Article  PubMed  Google Scholar 

  • Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kroger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jezequel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van De Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456(7219):239–244. doi:10.1038/nature07410

    Article  PubMed  CAS  Google Scholar 

  • Do H, Kim S-J, Kim HJ, Lee JH (2014) Structure-based characterization and antifreeze properties of a hyperactive ice-binding protein from the Antarctic bacterium Flavobacterium frigoris PS1. Acta Cryst D 70(4):1061–1073. doi:10.1107/S1399004714000996

    Article  CAS  Google Scholar 

  • Doucet D, Tyshenko MG, Kuiper MJ, Graether SP, Sykes BD, Daugulis AJ, Davies PL, Walker VK (2000) Structure-function relationships in spruce budworm antifreeze protein revealed by isoform diversity. Eur J Biochem 267(19):6082–6088. doi:10.1046/j.1432-1327.2000.01694.x

    Article  PubMed  CAS  Google Scholar 

  • Graether SP, Jia ZC (2001) Modeling Pseudomonas syringae ice-nucleation protein as a beta-helical protein. Biophys J 80(3):1169–1173

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Janech MG, Krell A, Mock T, Kang JS, Raymond JA (2006) Ice-binding proteins from sea ice diatoms (Bacillariophyceae). J Phycol 42(2):410–416. doi:10.1111/j.1529-8817.2006.00208.x

    Article  CAS  Google Scholar 

  • Kondo H, Hanada Y, Sugimoto H, Hoshino T, Garnham CP, Davies PL, Tsuda S (2012) Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. Proc Natl Acad Sci USA 109(24):9360–9365. doi:10.1073/pnas.1121607109

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Krembs C, Eicken H, Deming JW (2011) Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc Natl Acad Sci USA 108(9):3653–3658. doi:10.1073/pnas.1100701108

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kuiper MJ, Davies PL, Walker VK (2001) A theoretical model of a plant antifreeze protein from Lolium perenne. Biophys J 81(6):3560–3565

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lee JH, Park AK, Do H, Park KS, Moh SH, Chi YM, Kim HJ (2012) Structural basis for antifreeze activity of ice-binding protein from Arctic Yeast. J Biol Chem 287(14):11460–11468. doi:10.1074/jbc.M111.331835

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nosenko T, Bhattacharya D (2007) Horizontal gene transfer in chromalveolates. BMC Evol Biol 7:173. doi:10.1186/1471-2148-7-173

    Article  PubMed  PubMed Central  Google Scholar 

  • Raymond JA, Fritsen CH (2001) Semipurification and ice recrystallization inhibition activity of ice-active substances associated with Antarctic photosynthetic organisms. Cryobiology 43(1):63–70. doi:10.1006/cryo.2001.2341

    Article  PubMed  CAS  Google Scholar 

  • Raymond JA, Kim HJ (2012) Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS ONE 7(5):e35968. doi:10.1371/journal.pone.0035968

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Raymond JA, Morgan-Kiss R (2013) Separate origins of ice-binding proteins in Antarctic Chlamydomonas species. PLoS ONE 8(3):e59186. doi:10.1371/journal.pone.0059186

    Article  PubMed  PubMed Central  Google Scholar 

  • Raymond JA, Janech MG, Fritsen CH (2009) Novel ice-binding proteins from a psychrophilic Antarctic alga (Chlamydomonadaceae, Chlorophyceae). J Phycol 45(1):130–136. doi:10.1111/j.1529-8817.2008.00623.x

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr12

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

I thank the School of Life Sciences, University of Nevada, Las Vegas for providing laboratory facilities for conducting this work. I thank Alvaro Hernandez, Kristina Kruse, Kathleen Schegg and Casey Hall for sequencing and protein analyzes. I thank Arthur DeVries for many suggestions for improving the manuscript. Sequencing and protein analyzes at the University of Nevada were supported by grant #P20GM103440 from the National Institute of General Medical Sciences. Additional funding for this work was provided by the author.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James A. Raymond.

Additional information

Communicated by A. Driessen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Raymond, J.A. The ice-binding proteins of a snow alga, Chloromonas brevispina: probable acquisition by horizontal gene transfer. Extremophiles 18, 987–994 (2014). https://doi.org/10.1007/s00792-014-0668-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-014-0668-3

Keywords

Navigation