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The Under-explored Extracellular Proteome of Aero-Terrestrial Microalgae Provides Clues on Different Mechanisms of Desiccation Tolerance in Non-Model Organisms

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Abstract

Trebouxia sp. (TR9) and Coccomyxa simplex (Csol) are desiccation-tolerant lichen microalgae with different adaptive strategies in accordance with the prevailing conditions of their habitats. The remodelling of cell wall and extracellular polysaccharides depending on water availability are key elements in the tolerance to desiccation of both microalgae. Currently, there is no information about the extracellular proteins of these algae and other aero-terrestrial microalgae in response to limited water availability. To our knowledge, this is the first report on the proteins associated with the extracellular polymeric substances (EPS) of aero-terrestrial microalgae subjected to cyclic desiccation/rehydration. LC-MS/MS and bioinformatic analyses of the EPS-associated proteins in the two lichen microalgae submitted to four desiccation/rehydration cycles allowed the compilation of 111 and 121 identified proteins for TR9 and Csol, respectively. Both sets of EPS-associated proteins shared a variety of predicted biological functions but showed a constitutive expression in Csol and partially inducible in TR9. In both algae, the EPS-associated proteins included a number of proteins of unknown functions, some of which could be considered as small intrinsically disordered proteins related with desiccation-tolerant organisms. Differences in the composition and the expression pattern between the studied EPS-associated proteins would be oriented to preserve the biochemical and biophysical properties of the extracellular structures under the different conditions of water availability in which each alga thrives.

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References

  1. Costa OYA, Raaijmakers JM, Kuramae EE (2018) Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Front Microbiol 9:1636. https://doi.org/10.3389/fmicb.2018.01636

    Article  PubMed  PubMed Central  Google Scholar 

  2. Vincent D, Rafiqi M, Job D (2020) The multiple facets of plant-fungal interactions revealed through plant and fungal secretomics. Front Plant Sci 10:1626. https://doi.org/10.3389/fpls.2019.01626

    Article  PubMed  PubMed Central  Google Scholar 

  3. Krause C, Richter S, Knoll C, Jurgens G (2013) Plant secretome - from cellular process to biological activity. Biochim Biophys Acta 1834(11):2429–2441. https://doi.org/10.1016/j.bbapap.2013.03.024

    Article  CAS  PubMed  Google Scholar 

  4. Delaunois B, Jeandet P, Clément C, Baillieul F, Dorey S, Cordelier S (2014) Uncovering plant-pathogen crosstalk through apoplastic proteomic studies. Front Plant Sci 5:249. https://doi.org/10.3389/fpls.2014.00249

    Article  PubMed  PubMed Central  Google Scholar 

  5. Tanveer T, Shaheen K, Parveen S, Kazi AG, Ahmad P (2014) Plant secretomics: identification, isolation, and biological significance under environmental stress. Plant Signal Behav 9(8):e29426. https://doi.org/10.4161/psb.29426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Chen P, Jung NU, Giarola V, Bartels D (2020) The dynamic responses of cell walls in resurrection plants during dehydration and rehydration. Front Plant Sci 10:1698. https://doi.org/10.3389/fpls.2019.01698

    Article  PubMed  PubMed Central  Google Scholar 

  7. Pierre G, Delattre C, Dubessay P, Jubeau S, Vialleix C, Cadoret JP, Probert I, Michaud P (2019) What is in store for EPS microalgae in the next decade? Molecules 24(23):4296. https://doi.org/10.3390/molecules24234296

    Article  CAS  PubMed Central  Google Scholar 

  8. Xiao R, Zheng Y (2016) Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnol Adv 34(7):1225–1244. https://doi.org/10.1016/j.biotechadv.2016.08.004

    Article  CAS  PubMed  Google Scholar 

  9. Chiou Y, Hsieh M, Yeh H (2010) Effect of algal extracellular polymer substances on UF membrane fouling. Desalination 250:648–652. https://doi.org/10.1016/j.desal.2008.02.043

    Article  CAS  Google Scholar 

  10. Wang XQ, Yang PF, Liu Z, Liu WZ, Hu Y, Chen H, Kuang TY, Pei ZM, Shen SH, He YK (2009) Exploring the mechanism of Physcomitrella patens desiccation tolerance through a proteomic strategy. Plant Physiol 149(4):1739–1750. https://doi.org/10.1104/pp.108.131714

    Article  PubMed  PubMed Central  Google Scholar 

  11. Geun Goo B, Baek G, Jin Choi D, Il Park Y, Synytsya A, Bleha R, Ho Seong D, Lee C, Kweon Park J (2013) Characterization of a renewable extracellular polysaccharide from defatted microalgae Dunaliella tertiolecta. Bioresour Technol 129:343–350. https://doi.org/10.1016/j.biortech.2012.11.077

    Article  CAS  Google Scholar 

  12. Baba M, Suzuki I, Shiraiwa Y (2011) Proteomic analysis of high-CO(2)-inducible extracellular proteins in the unicellular green alga, Chlamydomonas reinhardtii. Plant Cell Physiol 52(8):1302–1314. https://doi.org/10.1093/pcp/pcr078

    Article  CAS  PubMed  Google Scholar 

  13. Terauchi M, Yamagishi T, Hanyuda T, Kawai H (2017) Genome-wide computational analysis of the secretome of brown algae (Phaeophyceae). Mar Genomics 32:49–59. https://doi.org/10.1016/j.margen.2016.12.002

    Article  PubMed  Google Scholar 

  14. Ruíz-May E, Sorensen I, Fei Z, Zhang S, Domozych DS, Rose JKC (2018) The secretome and N-glycosylation profiles of the Charophycean green alga, Penium margaritaceum, resemble those of Embryophytes. Proteomes 6(2). https://doi.org/10.3390/proteomes6020014

  15. Kranner I, Beckett R, Hochman A, Nash TH (2008) Desiccation-tolerance in lichens: a review. Bryologist 111:576–594. https://doi.org/10.1639/0007-2745-111.4.576

    Article  Google Scholar 

  16. Hell AF, Gasulla F, Gonzáez-Hourcade MA, del Campo EM, Centeno DC, Casano LM (2019) Tolerance to cyclic desiccation in lichen microalgae is related to habitat preference and involves specific priming of the antioxidant system. Plant Cell Physiol 60(8):1880–1891. https://doi.org/10.1093/pcp/pcz103

    Article  CAS  PubMed  Google Scholar 

  17. González-Hourcade M, Braga MR, del Campo EM, Ascaso C, Patino C, Casano LM (2020a) Ultrastructural and biochemical analyses reveal cell wall remodelling in lichen-forming microalgae submitted to cyclic desiccation-rehydration. Ann Bot 125(3):459–469. https://doi.org/10.1093/aob/mcz181

    Article  CAS  PubMed  Google Scholar 

  18. Casano LM, Braga MR, Álvarez R, del Campo EM, Barreno E (2015) Differences in the cell walls and extracellular polymers of the two Trebouxia microalgae coexisting in the lichen Ramalina farinacea are consistent with their distinct capacity to immobilize extracellular Pb. Plant Sci 236:195–204. https://doi.org/10.1016/j.plantsci.2015.04.003

    Article  CAS  PubMed  Google Scholar 

  19. González-Hourcade M, del Campo EM, Braga MR, Salgado A, Casano LM (2020b) Disentangling the role of extracellular polysaccharides in DT in lichen-forming microalgae. First evidence of sulfated polysaccharides and ancient sulfotransferase genes. Environ Microbiol (In press) 22:3096–3111. https://doi.org/10.1111/1462-2920.15043

    Article  CAS  PubMed  Google Scholar 

  20. Centeno DC, Hell AF, Braga MR, del Campo EM, Casano LM (2016) Contrasting strategies used by lichen microalgae to cope with desiccation-rehydration stress revealed by metabolite profiling and cell wall analysis. Environ Microbiol 18(5):1546–1560. https://doi.org/10.1111/1462-2920.13249

    Article  CAS  PubMed  Google Scholar 

  21. Oliveira P, Martins NM, Santos M, Couto NA, Wright PC, Tamagnini P (2015) The Anabaena sp. PCC 7120 exoproteome: taking a peek outside the box. Life (Basel) 5(1):130–163. https://doi.org/10.3390/life5010130

    Article  CAS  Google Scholar 

  22. Casano LM, del Campo EM, García-Breijo FJ, Reig-Arminana J, Gasulla F, Del Hoyo A, Guéra A, Barreno E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13(3):806–818. https://doi.org/10.1111/j.1462-2920.2010.02386.x

    Article  CAS  PubMed  Google Scholar 

  23. Malavasi V, Skaloud P, Rindi F, Tempesta S, Paoletti M, Pasqualetti M (2016) DNA-based taxonomy in ecologically versatile microalgae: a re-evaluation of the species concept within the coccoid green algal genus Coccomyxa (Trebouxiophyceae, Chlorophyta). PLoS One 11(3):e0151137. https://doi.org/10.1371/journal.pone.0151137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bold HC, Parker BC (1962) Some supplementary attributes in the classification of Chlorococcum species. Arch Mikrobiol 42:267–288. https://doi.org/10.1007/bf00422045

    Article  CAS  PubMed  Google Scholar 

  25. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999

    Article  CAS  PubMed  Google Scholar 

  26. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57(1):289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x

    Article  Google Scholar 

  27. Nielsen H, Tsirigos KD, Brunak S, von Heijne G (2019) A brief history of protein sorting prediction. Protein J 38(3):200–216. https://doi.org/10.1007/s10930-019-09838-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Almagro-Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H (2019) SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 37(4):420–423. https://doi.org/10.1038/s41587-019-0036-z

    Article  CAS  PubMed  Google Scholar 

  29. Hiller K, Grote A, Scheer M, Munch R, Jahn D (2004) PrediSi: prediction of signal peptides and their cleavage positions. Nucleic Acids Res 32(Web Server issue):W375–W379. https://doi.org/10.1093/nar/gkh378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kall L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server. Nucleic Acids Res 35(Web Server issue):W429–W432. https://doi.org/10.1093/nar/gkm256

    Article  PubMed  PubMed Central  Google Scholar 

  31. Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651. https://doi.org/10.1002/prot.21018

    Article  CAS  PubMed  Google Scholar 

  32. Lum G, Meinken J, Orr J, Frazier S, Min XJ (2014) PlantSecKB: the plant secretome and subcellular proteome knowledgebase. Comput Mol Biol 4(1):1–17. https://doi.org/10.5376/cmb.2014.04.0001

    Article  Google Scholar 

  33. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203. https://doi.org/10.1093/nar/gkw1129

    Article  CAS  PubMed  Google Scholar 

  34. 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, López R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9):1236–1240. https://doi.org/10.1093/bioinformatics/btu031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  36. Stothard P (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28(6):1102–1104. https://doi.org/10.2144/00286ir01

    Article  CAS  PubMed  Google Scholar 

  37. Herburger K, Holzinger A (2015) Localization and quantification of callose in the streptophyte green algae Zygnema and Klebsormidium: correlation with desiccation tolerance. Plant Cell Physiol 56:2259–2270. https://doi.org/10.1093/pcp/pcv139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Herburger K, Ryan LM, Popper ZA, Holzinger A (2018) Localisation and substrate specificities of transglycanases in charophyte algae relate to development and morphology. J Cell Sci 131:jcs203208. https://doi.org/10.1242/jcs.203208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yuan JS, Yang X, Lai J, Lin H, Cheng ZM, Nonogaki H, Chen F (2007) The endo-beta-mannanase gene families in Arabidopsis, rice, and poplar. Funct Integr Genomics 7(1):1–16. https://doi.org/10.1007/s10142-006-0034-3

    Article  CAS  PubMed  Google Scholar 

  40. Rosseto FR, Manzine LR, de Oliveira NM, Polikarpov I (2016) Biophysical and biochemical studies of a major endoglucanase secreted by Xanthomonas campestris pv. campestris. Enzym Microb Technol 91:1–7. https://doi.org/10.1016/j.enzmictec.2016.05.007

    Article  CAS  Google Scholar 

  41. Stone BA (2009) Chemistry of β-Glucans. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry, and biology of 1-3 beta glucans and related polysaccharides. Academic Press, pp 5–46

  42. Zhu J, Álvarez S, Marsh EL, Lenoble ME, Cho IJ, Sivaguru M, Chen S, Nguyen HT, Wu Y, Schachtman DP, Sharp RE (2007) Cell wall proteome in the maize primary root elongation zone. II Region-specific changes in water soluble and lightly ionically bound proteins under water deficit. Plant Physiol 145(4):1533–1548. https://doi.org/10.1104/pp.107.107250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ye T, Shi H, Wang Y, Chan Z (2015) Contrasting changes caused by drought and submergence stresses in bermudagrass (Cynodon dactylon). Front Plant Sci 6:951. https://doi.org/10.3389/fpls.2015.00951

    Article  PubMed  PubMed Central  Google Scholar 

  44. Li P, Zhang Y, Wu X, Liu Y (2018) Drought stress impact on leaf proteome variations of faba bean (Vicia faba L.) in the Qinghai-Tibet Plateau of China. 3 Biotech 8(2):110-018-1088-3. https://doi.org/10.1007/s13205-018-1088-3

    Article  Google Scholar 

  45. Carmo LST, Martins ACQ, Martins CCC, Passos MAS, Silva LP, Araujo ACG, Brasileiro ACM, Miller RNG, Guimaraes PM, Mehta A (2019) Comparative proteomics and gene expression analysis in Arachis duranensis reveal stress response proteins associated to drought tolerance. J Proteome 192:299–310. https://doi.org/10.1016/j.jprot.2018.09.011

    Article  CAS  Google Scholar 

  46. Gupta S, Mishra SK, Misra S, Pandey V, Agrawal L, Nautiyal CS, Chauhan PS (2020) Revealing the complexity of protein abundance in chickpea root under drought-stress using a comparative proteomics approach. Plant Physiol Biochem 151:88–102. https://doi.org/10.1016/j.plaphy.2020.03.005

    Article  CAS  PubMed  Google Scholar 

  47. Steinfeld L, Vafaei A, Rösner J, Merzendorfer H (2019) Chitin prevalence and function in bacteria, fungi and protists. Adv Exp Med Biol 1142:19–59. https://doi.org/10.1007/978-981-13-7318-3_3

    Article  CAS  PubMed  Google Scholar 

  48. Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115(2):327–334. https://doi.org/10.1104/pp.115.2.327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wang Q, Guo Q, Guo Y, Yang J, Wang M, Duan X, Niu J, Liu S, Zhang J, Lu Y, Hou Z, Miao W, Wang X, Kong W, Xu X, Wu Y, Rui Q, La H (2018) Arabidopsis subtilase SASP is involved in the regulation of ABA signaling and drought tolerance by interacting with OPEN STOMATA 1. J Exp Bot 69(18):4403–4417. https://doi.org/10.1093/jxb/ery205

    Article  CAS  PubMed  Google Scholar 

  50. Teale W, Palme K (2018) Naphthylphthalamic acid and the mechanism of polar auxin transport. J Exp Bot 69(2):303–312. https://doi.org/10.1093/jxb/erx323

    Article  CAS  PubMed  Google Scholar 

  51. Kidrič M, Sabotič J, Stevanović B (2014) Desiccation tolerance of the resurrection plant Ramonda serbica is associated with dehydration-dependent changes in levels of proteolytic activities. J Plant Physiol 171(12):998–1002. https://doi.org/10.1016/j.jplph.2014.03.011

    Article  CAS  PubMed  Google Scholar 

  52. Pichler G, Stöggl W, Candotto Carniel F, Muggia L, Ametrano CG, Holzinger A, Tretiach M, Kranner I (2020) Abundance and extracellular release of phytohormones in aero-terrestrial microalgae (Trebouxiophyceae, Chlorophyta) as a potential chemical signaling source. J Phycology (in press). https://doi.org/10.1111/jpy.13032

  53. Hajheidari M, Eivazi A, Buchanan BB, Wong JH, Majidi I, Salekdeh GH (2007) Proteomics uncovers a role for redox in drought tolerance in wheat. J Proteome Res 6(4):1451–1460. https://doi.org/10.1021/pr060570j

    Article  CAS  PubMed  Google Scholar 

  54. Pinheiro C, Kehr J, Ricardo CP (2005) Effect of water stress on lupin stem protein analysed by two-dimensional gel electrophoresis. Planta 221(5):716–728. https://doi.org/10.1007/s00425-004-1478-0

    Article  CAS  PubMed  Google Scholar 

  55. Bray EA (2002) Classification of genes differentially expressed during water-deficit stress in Arabidopsis thaliana: an analysis using microarray and differential expression data. Ann Bot 89 Spec No:803-811. https://doi.org/10.1093/aob/mcf104

  56. Schaller A (2004) A cut above the rest: the regulatory function of plant proteases. Planta 220(2):183–197. https://doi.org/10.1007/s00425-004-1407-2

    Article  CAS  PubMed  Google Scholar 

  57. Augusti A, Scartazza A, Navari-Izzo F, Sgherri CL, Stevanovic B, Brugnoli E (2001) Photosystem II photochemical efficiency, zeaxanthin and antioxidant contents in the poikilohydric Ramonda serbica during dehydration and rehydration. Photosynth Res 67(1-2):79–88. https://doi.org/10.1023/A:1010692632408

    Article  CAS  PubMed  Google Scholar 

  58. Sgherri C, Stevanovic B, Navari-Izzo F (2004) Role of phenolics in the antioxidative status of the resurrection plant Ramonda serbica during dehydration and rehydration. Physiol Plant 122(4):478–485. https://doi.org/10.1111/j.1399-3054.2004.00428.x

    Article  CAS  Google Scholar 

  59. Beckett RP, Minibayeva FV, Vylegzhanina NN, Tolpysheva T (2003) High rates of extracellular superoxide production by lichens in the suborder Peltigerineae correlate with indices of high metabolic activity. Plant Cell Environ 26(11):1827–1837. https://doi.org/10.1046/j.1365-3040.2003.01099.x

    Article  CAS  Google Scholar 

  60. Minibayeva F, Beckett RP (2001) High rates of extracellular superoxide production in bryophytes and lichens, and an oxidative burst in response to rehydration following desiccation. New Phytol 152(2):333–341. https://doi.org/10.1046/j.0028-646X.2001.00256.x

    Article  CAS  Google Scholar 

  61. Jovanović Ž, Rakić T, Stevanović B, Radović S (2011) Characterization of oxidative and antioxidative events during dehydration and rehydration of resurrection plant Ramonda nathaliae. Plant Growth Regul 64(3):231–240. https://doi.org/10.1007/s10725-011-9563-4

    Article  CAS  Google Scholar 

  62. Kärkönen A, Kuchitsu K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112:22–32. https://doi.org/10.1016/j.phytochem.2014.09.016

    Article  CAS  PubMed  Google Scholar 

  63. Vanden Wymelenberg A, Sabat G, Mozuch M, Kersten PJ, Cullen D, Blanchette RA (2006) Structure, organization, and transcriptional regulation of a family of copper radical oxidase genes in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 72(7):4871–4877. https://doi.org/10.1128/AEM.00375-06

    Article  CAS  Google Scholar 

  64. Davidson R, Reeves P, Manosalva P, Leach J (2009) Germins: a diverse protein family important for crop improvement. Plant Sci 177(6):499–510. https://doi.org/10.1016/j.plantsci.2009.08.012

    Article  CAS  Google Scholar 

  65. Pei Y, Li X, Zhu Y, Ge X, Sun Y, Liu N, Jia Y, Li F, Hou Y (2019) GhABP19, a novel germin-like protein from Gossypium hirsutum, plays an important role in the regulation of resistance to Verticillium and Fusarium wilt pathogens. Front Plant Sci 10:583. https://doi.org/10.3389/fpls.2019.00583

    Article  PubMed  PubMed Central  Google Scholar 

  66. Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2˙−, H2O2, and ˙OH) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136(2):3114–3123. https://doi.org/10.1104/pp.104.044784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Müller K, Linkies A, Vreeburg RAM, Fry SC, Krieger-Liszkay A, Leubner-Metzger G (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150(4):1855–1865. https://doi.org/10.1104/pp.109.139204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: Implications for the control of elongation growth. Plant J 28:679–688. https://doi.org/10.1046/j.1365-313x.2001.01187.x

    Article  CAS  PubMed  Google Scholar 

  69. Smukalla S, Caldara M, Pochet N, Beauvais A, Guadagnini S, Yan C, Vinces MD, Jansen A, Prevost MC, Latgé JP, Fink GR, Foster KR, Verstrepen KJ (2008) FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cells 135:726–737. https://doi.org/10.1016/j.cell.2008.09.037

    Article  CAS  Google Scholar 

  70. Cardon ZG, Peredo EL, Dohnalkova AC, Gershone HL, Bezanilla M (2018) A model suite of green algae within the Scenedesmaceae for investigating contrasting desiccation tolerance and morphology. J Cell Sci 131(7):jcs212233. https://doi.org/10.1242/jcs.212233

    Article  CAS  PubMed  Google Scholar 

  71. Domozych DS, Domozych CE (2014) Multicellularity in green algae: upsizing in a walled complex. Front Plant Sci 5:649. https://doi.org/10.3389/fpls.2014.00649

    Article  PubMed  PubMed Central  Google Scholar 

  72. Alsufyani T, Califano G, Deicke M, Grueneberg J, Weiss A, Engelen AH, Kwantes M, Mohr JF, Ulrich JF, Wichard T (2020) Macroalgal-bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva (Chlorophyta). J Exp Bot 71(11):3340–3349. https://doi.org/10.1093/jxb/eraa066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Boothby TC, Pielak GJ (2017) Intrinsically disordered proteins and DT: elucidating functional and mechanistic underpinnings of anhydrobiosis. Bioessays 39(11):10. https://doi.org/10.1002/bies.201700119

    Article  CAS  Google Scholar 

  74. Koshland D, Tapia H (2019) Desiccation tolerance: an unusual window into stress biology. Mol Biol Cell 30(6):737–741. https://doi.org/10.1091/mbc.E17-04-0257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Schatz D, Rosenwasser S, Malitsky S, Wolf SG, Feldmesser E, Vardi A (2017) Communication via extracellular vesicles enhances viral infection of a cosmopolitan alga. Nat Microbiol 2(11):1485–1492. https://doi.org/10.1038/s41564-017-0024-3

    Article  CAS  PubMed  Google Scholar 

  76. Rutter BD, Innes RW (2017) Extracellular vesicles isolated from the leaf apoplast carry stress-response proteins. Plant Physiol 173(1):728–741. https://doi.org/10.1104/pp.16.01253

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by a grant from the Spanish Ministry of Science, Innovation and Universities [CGL2016-80259-P]. We thank the Proteomics Unit of Complutense University of Madrid, a member of ProteoRed (supported by Grant PRB3 [IPT17/0019 - ISCIII-SGEFI / ERDF]) for the LC-MS/MS analyses of EPS-associated proteins from TR9 and Csol algae, and Gabriel Casano for the English revision of the manuscript.

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  1. Department of Life Sciences, University of Alcalá, 28805, Alcalá de Henares, Madrid, Spain

    María González-Hourcade, Eva M. del Campo & Leonardo M. Casano

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  1. María González-Hourcade
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  2. Eva M. del Campo
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  3. Leonardo M. Casano
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Correspondence to Eva M. del Campo.

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González-Hourcade, M., del Campo, E.M. & Casano, L.M. The Under-explored Extracellular Proteome of Aero-Terrestrial Microalgae Provides Clues on Different Mechanisms of Desiccation Tolerance in Non-Model Organisms. Microb Ecol 81, 437–453 (2021). https://doi.org/10.1007/s00248-020-01604-8

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  • DOI: https://doi.org/10.1007/s00248-020-01604-8

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