My research within the subject photosynthesis currently has developed into two different projects: 1. Investigating the potential of Nordic microalgae for wastewater reclamation and biomass generation and 2. Finding the function of plant proteases. Research objects in my group range from cyanobacteria, via green microalgae and cryptomonad algae to higher plants.

Christiane Funk 1150 766

Wastewater reclamation and biomass generation by Nordic microalgae

With the expanding human population, we will need more food, more fuel and more water. At the same time, we have to reduce CO2 emissions by over 80%. One approach to address this problem is to recycle CO2 for fuel- or chemical-production using photosynthesis. Photosynthetic organisms use solar energy to incorporate atmospheric CO2 into organic molecules. We let microalgae perform photosynthesis and at the same time clean municipal and industrial wastewater. The algal biomass then can be used for biofuel, biogas, biofertilizer or even bioplastic. Our challenge is the sub-arctic climate we have in Northern Sweden with low temperatures and short-day lengths. Therefore, we investigate the potential of local, natural algal strains. We test their performance in cleaning wastewater, analyze their biomass and investigate, how to prolong their growth phase.

Plant proteases

Proteases are proteins that break down other proteins. They are involved in many different biological functions, e.g. the digestion of our food, cleaning the cell from malfunctioning proteins or cell signaling. Even though hundreds of proteases are encoded in the genomes of various plants, their biological roles are mostly unknown. Using molecular biological and biochemical methods, we try to find identify the function of some of them. Metacaspases, for example, are proteases thought to be involved in programmed cell death (PCD), the genetically encoded process leading to suicide of specific cells or tissues. In single-cell algae and cyanobacteria the necessity for PCD is less obvious, still these microorganisms contain metacaspases. The aim of our research is to investigate the broad network of PCD in photosynthetic single-cell organisms and at the same time to perform detailed functional, structural and evolutionary studies of the metacaspase homologues.

Microalgae and chlorophyll fluorescence in Arabidopsis_ ChristianeFunkA) Various green microalgae found in municipal wastewater; B) Scanning electron microscope (SEM) image of the green microalga C. vulgaris 13-1 and its symbiotic bacterium Rhizobium sp. at 50 K magnification (Photos: Lorenza Ferro); C) Electron microscopy image of the cyanobacterium Synechocystis sp. 6803 (Photo: Tania Tibiletti); D) Chlorophyll fluorescence emitted from Arabidopsis thaliana leaves (Photo: Laxmi Mishra)

sweden_greySvensk sammanfattning

Publication list

  1. Screening Suitability of Northern Hemisphere Algal Strains for Heterotrophic Cultivation and Fatty Acid Methyl Ester Production
    Molecules. 2020, 25(9):E2107
  2. Classification and Nomenclature of Metacaspases and Paracaspases: No More Confusion with Caspases
    Mol Cell. 2020, 77(5):927-929
  3. Uptake Kinetics of Methylmercury in a Freshwater Alga Exposed to Methylmercury Complexes with Environmentally Relevant Thiols
    Environmental Science & Technology 2019, 53 (23): 13757-13766
  4. Growth performance and nutrient removal of a Chlorella vulgaris-Rhizobium sp. co-culture during mixotrophic feed-batch cultivation in synthetic wastewater
    Algal Research 2019, 4: 101690
  5. Statistical Methods for Rapid Quantification of Proteins, Lipids, and Carbohydrates in Nordic Microalgal Species Using ATR–FTIR Spectroscopy
    Molecules 2019, 24(18): 3237
  6. Use of pulsed electric field permeabilization to extract astaxanthin from the Nordic microalga Haematococcus pluvialis
    Bioresour Technol. 2019, 289: 121694
  7. DEG10 contributes to mitochondrial proteostasis, root growth, and seed yield in Arabidopsis
    J Exp Bot. 2019, 70(19): 5423-5436
  8. Extra-plastidial degradation of chlorophyll and photosystem I in tobacco leaves involving 'senescence-associated vacuoles'
    Plant J. 2019, 99(3): 465-477
  9. Functional expression of Gloeobacter rhodopsin in PSI-less Synechocystis sp. PCC 6803
    Front Bioeng Biotechnol. 2019 7: 67
  10. Evolution and structural diversity of metacaspases
    J Exp Bot. 2019, 70(7): 2039-2047
  11. Phylogenetic Distribution and Diversity of Bacterial Pseudo-Orthocaspases Underline Their Putative Role in Photosynthesis
    Front Plant Sci. 2019, 10: 293
  12. Reduced expression of the proteolytically inactive FtsH members has impacts on the Darwinian fitness of Arabidopsis thaliana
    J Exp Bot 2019, 70(7): 2173-2184
  13. Microalgae Cultivation for the Biotransformation of Birch Wood Hydrolysate and Dairy Effluent
    Catalysts 2019, 9(2): 150
  14. Elucidating the symbiotic interactions between a locally isolated microalga Chlorella vulgaris and its co-occurring bacterium Rhizobium sp. in synthetic municipal wastewater
    J Appl Phycol 2019, 31(4): 2299-2310
  15. Green Bioplastics as Part of a Circular Bioeconomy
    Trends in Plant Science 2019, 24(3): 237-249
  16. Northern green algae have the capacity to remove active pharmaceutical ingredients
    Ecotoxicol Environ Saf. 2019, 170:644-656
  17. Combining retinal-based and chlorophyll-based (oxygenic) photosynthesis: Proteorhodopsin expression increases growth rate and fitness of a ∆PSI strain of Synechocystis sp. PCC6803
    Metab Eng. 2019, 52:68-76
  18. Subarctic microalgal strains treat wastewater and produce biomass at low temperature and short photoperiod
    Algal Research 2018, 35: 160-167
  19. Isolation and characterization of microalgal strains for biomass production and wastewater reclamation in Northern Sweden
    Algal Research 2018, 32: 44-53
  20. Algal Biomass from Wastewater and Flue Gases as a Source of Bioenergy
    Energies 2018, 11(3): 664
  21. Stable accumulation of photosystem II requires ONE-HELIX PROTEIN1 (OHP1) of the light harvesting-like family
    Plant Physiology 2018, 176 (3):2277-2291
  22. The stress-induced SCP/HLIP family of small light-harvesting-like proteins (ScpABCDE) protects Photosystem II from photoinhibitory damages in the cyanobacterium Synechocystis sp. PCC 6803
    Photosynth Res. 2018, 135(1-3):103-114
  23. Structural and functional diversity of caspase homologues in non-metazoan organisms
    Protoplasma 2018, 255(1):387-397
  24. Type III metacaspases: calcium-dependent activity proposes new function for the p10 domain
    New Phytol. 2018, 218(3):1179-1191
  25. Proteomic analysis of the phycobiliprotein antenna of the cryptophyte alga Guillardia theta cultured under different light intensities
    Photosynth Res. 2018, 135(1-3):149-163
  26. The HhoA protease from Synechocystis sp. PCC 6803 - novel insights into structure and activity regulation
    J Struct Biol. 2017, 198(3):147-153
  27. Antibiotic Disc Assay for Measuring Cell Wall Function in Synechocystis sp. PCC6803
    Bio-protocol 2016, 6(24): e2071
  28. Deletion of FtsH11 protease has impact on chloroplast structure and function in Arabidopsis thaliana when grown under continuous light
    Plant Cell Environ. 2016, 39(11):2530-2544
  29. Lack of FTSH4 Protease Affects Protein Carbonylation, Mitochondrial Morphology, and Phospholipid Content in Mitochondria of Arabidopsis: New Insights into a Complex Interplay
    Plant Physiol. 2016, 171(4):2516-35
  30. The PsbY protein of Arabidopsis Photosystem II is important for the redox control of Cytochrome b559
    Biochim Biophys Acta. 2016 May 21. pii: S0005-2728(16)30536-9 [Epub ahead of print]
  31. Insights into the Cyanobacterial Deg/HtrA Proteases
    Front Plant Sci. 2016, 7: 694
  32. Deletion of the gene family of small chlorophyll-binding proteins (ScpABCDE) offsets C/N homeostasis in Synechocystis PCC 6803
    Biochim Biophys Acta. 2016, 1857(4):396-407
  33. Regulation of the scp Genes in the Cyanobacterium Synechocystis sp. PCC 6803-What is New?
    Molecules. 2015, 20(8):14621-37
  34. Presence of state transitions in the cryptophyte alga Guillardia theta
    J Exp Bot. 2015, 66(20): 6461-70
  35. Inactivation of the Deg protease family in the cyanobacterium Synechocystis sp. PCC 6803 has impact on the outer cell layers
    J Photochem Photobiol B. 2015,152(Pt B): 383-94
  36. Proteomic approaches to identify substrates of the three Deg/HtrA proteases of the cyanobacterium Synechocystis sp. PCC 6803
    Biochem J. 2015, 15;468(3):373-84
  37. Synergy: A Web Resource for Exploring Gene Regulation in Synechocystis sp. PCC6803
    PLoS One. 2014 Nov 24;9(11):e113496
  38. Metabolomic analysis of extreme freezing tolerance in Siberian spruce (Picea obovata)
    New Phytol. 2014, 204(3):545-555
  39. Family-wide characterization of Matrix Metallo-proteinases from Arabidopsis thaliana reveals their distinct proteolytic activity and cleavage site specificity
    Biochem J. 2013 Oct 25. [Epub ahead of print]
  40. Storm P, Tibiletti T, Hall M, Funk C
    Refolding and Enzyme Kinetic Studies on the Ferrochelatase of the Cyanobacterium Synechocystis sp. PCC 6803
    PLoS ONE 2013 8(2):e55569
  41. Miranda H, Cheregi O, Netotea S, Hvidsten TR, Moritz T, Funk C
    Co-expression analysis, proteomic and metabolomic study on the impact of a Deg/HtrA protease triple mutant in Synechocystis sp. PCC 6803 exposed to temperature and high light stress
    J. of Proteomics 2013, 78:94-311
  42. Cheregi O, Vermaas W, Funk C
    The search for new chlorophyll-binding proteins in the cyanobacterium Synechocystis sp. PCC 6803
    J Biotechnol. 2012 Jul 1. [Epub ahead of print]
  43. Roberts IN, Lam XT, Miranda H, Kieselbach T, Funk C
    Degradation of PsbO by the Deg Protease HhoA Is Thioredoxin Dependent
    PLoS One. 2012;7(9):e45713 Epub Sep 19
  44. Roberts IN, Caputo C, Criado MV, Funk C
    Senescence-associated proteases in plants
    Physiol Plant. 2012 May;145(1):130-9
  45. Wagner R, Aigner H, Funk C
    FtsH proteases located in the plant chloroplast
    Physiol Plant. 2012 May;145(1):203-14
  46. Mishra Y, Johansson Jankanpaa H, Kiss AZ, Funk C, Schroder WP, Jansson S
    Arabidopsis plants grown in the field and climate chambers significantly differ in leaf morphology and photosystem components
    BMC Plant Biology 2012, 12:6
  47. Matrix metalloproteinases in plants: A brief overview
    Physiol Plant: 2012, 145(1):196-202
  48. Crystal structure of the TL29 protein from Arabidopsis thaliana: An APX homolog without peroxidase activity
    J Struct Biol.: 2011 176(1):24-31
  49. Shi L, Hall M, Funk C, Schröder WP
    Photosystem II, a growing complex: Updates on newly discovered components and low molecular mass proteins
    Biochimica et Biophysica Acta - Bioenergetics: 1817 (2012), pp. 13-25
  50. Ådén J, Wallgren M, Storm P, Weise CF, Christiansen A, Schröder WP, Funk C, Wolf-Watz M
    Extraordinary μs–ms backbone dynamics in Arabidopsis thaliana peroxiredoxin Q
    Biochimica et Biophysica Acta - Proteins & Proteomics: 1814, 1880-1890
  51. Funk C, Alami M, Tibiletti T, Green BR
    High light stress and the one-helix LHC-like proteins of the cryptophyte Guillardia theta
    Biochim Biophys Acta.: 2011, 1807(7):841-6
  52. Hernandez-Prieto MA, Tibiletti T, Abasova L, Kirilovsky D, Vass I, Funk C
    The small CAB-like proteins of the cyanobacterium Synechocystis sp. PCC 6803: their involvement in chlorophyll biogenesis for Photosystem II
    Biochim Biophys Acta.: 2011, 1807(9):1143-51
  53. Wagner R, Aigner H, Pruzinska A, Jänkänpää HJ, Jansson S, Funk C
    Fitness analyses of Arabidopsis thaliana mutants depleted of FtsH metalloproteases and characterization of three FtsH6 deletion mutants exposed to high light stress, senescence and chilling
    The New Phytologist: 2011, 191:449-458
  54. Huesgen PF, Miranda H, Lam X, Perthold M, Schuhmann H, Adamska I, Funk C
    Recombinant Deg/HtrA proteases from Synechocystis sp. PCC 6803 differ in substrate specificity, biochemical characteristics and mechanism
    Biochem J.: 2011, 435(3):733-42
  55. Garcia-Cerdán JG, Kovács L, Tóth T, Kereiche S, Avseeva E, Boekema EJ, Mamedov F, Funk C, Schröder WP
    The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants
    The Plant Journal: 2011 65: 368-381
  56. Granlund I, Storm P, Schubert M, Garcia-Cerdan JG, Funk C, Schröder WP
    The TL29 protein is lumen located associated with Photosystem II and not an ascorbate peroxidase
    Plant and Cell Physiology: 2009 50:1898-1910
  57. Garcia-Cerdin JG, Sveshnikov D, Dewer D., Jansson S, Funk C, Schröder WP
    Antisense inhibition of the PsbX protein affects PSII integrity in higher plant Arabidopsis thaliana
    Plant and Cell Physiology: 2009 50(2):191-202
  58. Storm P, Hernandez-Prieto MA, Eggink LL, Hoober JK, Funk C
    The small CAB-like proteins of Synechocystis sp. PCC 6803 bind chlorophyll : In vitro pigment reconstitution studies on one-helix light-harvesting-like proteins
    Photosynthesis Research: 2008 98(1-3):479-488
  59. Sveshnikov D, Funk C, Schröder WP
    The PsbP-like protein (sll1418) of Synechocystis sp. PCC 6803 stabilises the donor side of Photosystem II
    Photosynthesis Research: 2008 93:101-109
  60. Garcia-Lorenzo M, Zelisko A, Jackowski G, Funk C
    Degradation of the main photosystem II light-harvesting complex
    Photochemical and Photobiological Sciences:2005 4:1065-1071
  61. Kufryk G, Hernandez-Prieto MA, Kieselbach T, Miranda H, Vermaas W, Funk C
    Association of small CAB-like proteins (SCPs) of Synechocystis sp. PCC 6803 with Photosystem II

    Photosynthesis Research: 2008 95:135-145
  62. Garcia-Lorenzo M, Sjödin A, Jansson S, Funk C
    Protease gene families in Populus and Arabidopsis
    BMC Plant Biology 2006 6: 30, 24 pp.
  63. Yao D, Kieselbach T, Komenda J, Promnares K, Prieto MAH, Tichy M, Vermaas W, Funk C
    Localization of the Small CAB-like Proeins in Photosystem II
    J Biol Chem 2007 282:267-276
  64. Demmig-Adams B, Ebbert V, Mellman DL, Mueh KE, Schaffer L, Funk C, Zarter CR, Adamska I, Jansson S, Iii WWA
    Modulation of PsbS and flexible vs sustained energy dissipation by light environment in different species
    Physiologia Plantarum: 2006 127:670-680
  65. Sveshnikov D, Ensminger I, Ivanov AG, Campbell D, Lloyd J, Funk C, Huner NPA, Oquist G
    Excitation energy partitioning and quenching during cold acclimation in Scots pine
    Tree Physiology: 2006 26:325-336
  66. Moreau C, Aksenov N, Lorenzo MG, Segerman B, Funk C, Nilsson P, Jansson S, Tuominen H
    A genomic approach to investigate developmental cell death in woody tissues of Populus trees
    Genome Biology: 2005 6:R34
  67. Ishikawa Y, Schroder WP, Funk C
    Functional analysis of the PsbP-like protein (sll1418) in Synechocystis sp. PCC 6803
    Photosynth Res: 2005 84:257-262
  68. Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S, Funk C
    AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence
    Proceedings of the National Academy of Sciences of the United States of America: 2005 102:13699-13704-
  69. Ensminger I, Sveshnikov D, Campbell DA, Funk C, Jansson S, Lloyd J, Shibistova O, Oquist G
    Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests
    Global Change Biology: 2004 10:995-1008
  70. Xu H, Vavilin D, Funk C, Vermaas W
    Multiple deletions of small Cab-like proteins in the cyanobacterium Synechocystis sp. PCC 6803: consequences for pigment biosynthesis and accumulation
    J Biol Chem: 2004 279:27971-27979
  71. Dedic R, Promnares K, Psencik J, Svoboda A, Korinek M, Tichy M, Komenda J, Funk C, Hala J
    Hole burning study of cyanobacterial Photosystem II complexes differing in the content of small putative chlorophyll-binding proteins
    Journal of Luminescence: 2004 107:230-235
  72. Huang F, Hedman E, Funk C, Kieselbach T, Schroder WP, Norling B
    Isolation of outer membrane of Synechocystis sp PCC 6803 and its proteomic characterization
    Molecular & Cellular Proteomics: 2004 3:586-595
  73. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T
    Proteome map of the chloroplast lumen of Arabidopsis thaliana (vol 277, pg 8354, 2002)
    Journal of Biological Chemistry: 2003 278:13590-13590
  74. Schofield SC, Campbell DA, Funk C, MacKenzie TDB
    Changes in macromolecular allocation in nondividing algal symbionts allow for photosynthetic acclimation in the lichen Lobaria pulmonaria
    New Phytologist: 2003 159:709-718
  75. Kieselbach T, Funk C
    The family of Deg/HtrA proteases: from Escherichia coli to Arabidopsis
    Physiologia Plantarum: 2003 119:337-346
  76. Noren H, Svensson P, Stegmark R, Funk C, Adamska I, Andersson B
    Expression of the early light-induced protein but not the PsbS protein is influenced by low temperature and depends on the developmental stage of the plant in field-grown pea cultivars
    Plant Cell and Environment: 2003 26:245-253
  77. Thidholm E, Lindstrom V, Tissier C, Robinson C, Schroder WP, Funk C
    Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the photosystem II dimer
    Febs Letters: 2002 513:217-222
  78. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T
    Proteome map of the chloroplast lumen of Arabidopsis thaliana
    J Biol Chem: 2002 277:8354-8365
  79. Clarke SM, Funk C, Hendry GS, Shand JA, Wydrzynski T, Eaton-Rye JJ
    Amino acid deletions in the cytosolic domains of the chlorophyll alpha-binding protein CP47 slow Q(A)(-) oxidation and/or prevent the assembly of Photosystem II
    Plant Molecular Biology: 2002 50:563-572
  80. Xu H, Vavilin D, Funk C, Vermaas W
    Small Cab-like proteins regulating tetrapyrrole biosynthesis in the cyanobacterium Synechocystis sp PCC 6803
    Plant Molecular Biology: 2002 49:149-160
  81. Funk C, Wiklund R, Schroder WP, Jansson C
    D1 ' centers are less efficient than normal photosystem II centers
    Febs Letters: 2001 505:113-117
  82. Chow WS, Funk C, Hope AB, Govindjee
    Greening of intermittent-light-grown bean plants in continuous light: thylakoid components in relation to photosynthetic performance and capacity for photoprotection
    Indian J Biochem Biophys: 2000 37:395-404
  83. Nield J, Funk C, Barber J
    Supermolecular structure of photosystem II and location of the PsbS protein
    Philosophical Transactions of the Royal Society of London Series B-Biological Sciences: 2000 355:1337-1343
  84. Schoefs B, Bertrand M, Funk C
    Photoactive protochlorophyllide regeneration in cotyledons and leaves from higher plants
    Photochem Photobiol: 2000 72:660-668
  85. Funk C
    Functional analysis of the PsbX protein by deletion of the corresponding gene in Synechocystis sp PCC 6803
    Plant Molecular Biology: 2000 44:815-827
  86. Funk C, Vermaas W
    A cyanobacterial gene family coding for single-helix proteins resembling part of the light-harvesting proteins from higher plants
    Biochemistry: 1999 38:9397-9404
  87. Vermaas W, Xu H, He QF, Funk C, Paulsen H
    Chlorophyll-binding proteins in cyanobacteria
    Photochemistry and Photobiology: 1999 69:71S-72S
  88. Funk C, Schroder WP, Salih G, Wiklund R, Jansson C
    Engineering of N-terminal threonines in the D1 protein impairs photosystem II energy transfer in Synechocystis 6803
    Febs Letters: 1998 436:434-438
  89. Lindahl M, Funk C, Webster J, Bingsmark S, Adamska I, Andersson B
    Expression of ELIPs and PS II-S protein in spinach during acclimative reduction of the Photosystem II antenna in response to increased tight intensities
    Photosynthesis Research: 1997 54:227-236
  90. Adamska I, Funk C, Renger G, Andersson B
    Developmental regulation of the PsbS gene expression in spinach seedlings: the role of phytochrome
    Plant Mol Biol: 1996 31:793-802
  91. Funk C, Schroder WP, Napiwotzki A, Tjus SE, Renger G, Andersson B
    The Psii-S Protein of Higher-Plants - a New-Type of Pigment-Binding Protein
    Biochemistry: 1995 34:11133-11141
  92. Funk C, Adamska I, Green BR, Andersson B, Renger G
    The Nuclear-Encoded Chlorophyll-Binding Photosystem-Ii-S Protein Is Stable in the Absence of Pigments
    Journal of Biological Chemistry: 1995 270:30141-30147
  93. Irrgang KD, Shi LX, Funk C, Schroder WP
    A Nuclear-Encoded Subunit of the Photosystem-Ii Reaction-Center
    Journal of Biological Chemistry: 1995 270:17588-17593
  94. Funk C, Schroder WP, Green BR, Renger G, Andersson B
    The Intrinsic 22 Kda Protein Is a Chlorophyll-Binding Subunit of Photosystem-Ii
    Febs Letters: 1994 342:261-266