Acquisition and metabolism of carbon in the ochrophyta other than diatoms

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 372, Issue 1728, 2017, Pages

  Raven, John A ^a,b   Giordano, Mario ^c,d  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^d INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

Brown algae; CO2 concentrating mechanism; Diffusive CO2 entry; Inorganic carbon; Photosynthesis; Rubisco

Indexed keywords

BROWN ALGA; CARBON DIOXIDE; CARBON FIXATION; DIATOM; ENZYME; EUKARYOTE; INORGANIC CARBON; METABOLISM; PHOTOSYNTHESIS;

ALGAE; BACILLARIOPHYTA; CHRYSOPHYCEAE; EUSTIGMATOPHYCEAE; FUCALES; PHAEOPHYCEAE; STRAMENOCHROMA; SYNURALES;

CARBON; INORGANIC COMPOUND;

CLASSIFICATION; METABOLISM; PHYLOGENY; STRAMENOPILE;

CARBON; INORGANIC CHEMICALS; PHYLOGENY; STRAMENOPILES;

EID: 85024858334     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2016.0400     Document Type: Review

References (141)

1. Raven JA, Beardall J, Larkum AWD, Sánchez-Baracaldo P. 2013 Interactions of photosynthesis with genome size and function. Phil. Trans. R. Soc. B 368, 20120264. (doi:10.1098/rstb.2012.0264)
2. Beakes GW, Glockling SL, Sekimoto S. 2012 The evolutionary phylogeny of the oomycete ‘fungi’. Protoplasma 249, 3–19. (doi:10.1007/s00709-011-0269-2)
3. Maberly SC, Ball LA, Raven JA, Súltmeyer D. 2009 Inorganic carbon acquisition by chrysophytes. J. Phycol. 49, 1052–1061. (doi:10.1111/j.1529-8817.2009.00734.x)
4. Wilken S, Schuurmans JM, Matthijs HCP. 2014 Do mixotrophs grow as photoheterotrophs? Photophysiological acclimation of the chrysophyte Ochromonas danica after feeding. New. Phytol. 204, 882–889. (doi:10.1111/nph.12975)
5. Yang EC, Boo GH, Kim HJ, Cho SM, Boo SH, Anderson RA, Yoon HW. 2012 Supermatrix data highlight the phylogenetic relationships of photosynthetic stramenopiles. Protist 163, 217–231. (doi:10.1016/j.protis.2011.08.001)
6. Baurain D et al. 2010 Phylogenetic evidence for separate acquisition of plastids in cryptophytes, haptophytes and stramenopiles. Mol. Biol. Evol. 22, 1698–1709. (doi:10.1093/molbev/msq059)
7. Brown JW, Sorhannus U. 2010 A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): substantive underestimation of putative fossil ages. PLoS ONE 5, e12759. (doi:10.1371/journal.pone.0012759)
8. Schmidt M, Horn S, Flieger K, Ehlers K, Wilhelm C, Schnetter R. 2012 Synchroma pusillum sp. nov. and other new algal isolates with chloroplast complexes confirm the Synchromophyceae (Ochrophyta) as a widely distributed group of amoeboid algae. Protist 163, 544–559. (doi:10.1016/j.protis.2011.11.009)
9. 2 -concentrating mechanisms in algae. Can. J. Bot. 76, 1052–1071. (doi:10.1139/b98-074)
10. Roberts K, Granum E, Leegood RC, Raven JA. 2007 Carbon acquisition by diatoms. Photosynth. Res. 93, 79–88. (doi:10.1007/s11120-007-9172-2)
11. Nakajima K, Tanaka A, Matsuda Y. 2013 SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc. Natl Acad. Sci. USA 110, 1767–1772. (doi:10.1073/pnas. 1216234110)
12. 2 -concentrating mechanisms in a marine diatom, Thalassiosira pseudonana. New Phytol. 209, 1417–1427. (doi:10.1111/nph. 13728)
13. Round FE, Crawford RM, Mann DG. 1990 Diatoms: biology and morphology of the genera. Cambridge, UK: Cambridge University Press.
14. Rousseaux CS, Gregg WW. 2014 Interannual variation in phytoplankton primary production at a global scale. Remote Sens. 6, 1–19. (doi:10.3390/rs6010001)
15. Silberfeld T, Leigh JW, Vergruggen H, Cruaud C, de Reviers B, Rousseau F. 2014 A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the ‘brown algal crown radiation’. Mol. Phylogenet. Evol. 56, 659–674. (doi:10.1016/j.ympev.2010.04.020)
16. Hurd CL, Harrison PJ, Bischof K, Lobban CS. 2014 Seaweed ecology and physiology, 2nd edn. Cambridge, UK: Cambridge University Press.
17. Saxby-Rouen KJ, Leadbeater BS, Reynolds CS. 1997 The relationship between the growth of Synura petersenii (Synurophyceae) to photon flux density, temperature and pH. Phycologia 36, 233–243. (doi:10.2216/i0031-8884-36-3-233.1)
18. Nixdorf B, Mischke U. 1998 Chrysophytes and chlamydomonads: pioneer colonists in extremely acid mining lakes (pH < 3) in Lusatia (Germany). Hydrobiologia 369/370, 315–327. (doi:10.1023/A:1017010229136)
19. Wolfe AP, Siver PA. 2013 A hypothesis linking chrysophyte microfossils to lake carbon dynamics on ecological and evolutionary time scales. Glob. Planet. Chang. 111, 189–198. (doi:10.1016/j. gloplacha.2013.09.014)
20. Sukenik A, Beardall J, Kromkamp J, Kopecký J, Macojídek J, Bergegeijk S, Gabon S, Shahan E, Yamishon A. 2009 Photosynthetic performance of outdoor Nannochloropsis mass cultures under a wide range of environmental conditions. Aquat. Microb. Ecol. 56, 297–308. (doi:10.3354/ame01309)
21. Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Sattlage RE, Boore JL, Rosewitz MC. 2011 Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropsis gaditana. Nat. Commun. 3, 686. (doi:10.1038/ncomms1688)
22. Vieler A et al. 2012 Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS ONE 8, e1003064. (doi:10. 1371/journal.pgen.1003064)
23. Tang YZ, Koch F, Gobler CJ. 2010 Most harmful algae are vitamin B1 and B12 auxotrophs. Proc. Natl Acad. Sci. USA 107, 20 756–20 761. (doi:10.1073/pnas.1009566107)
24. Raven JA, Beardall J, Giordano M. 2014 Energy costs of concentrating mechanisms in aquatic organisms. Photosynth. Res. 121, 111–124. (doi:10.1007/s11120-013-9962-7)
25. 2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Phil. Trans. R Soc. B 367, 493–507. (doi:10.1098/rstb.2011.0212)
26. 2 concentrating mechanisms and environmental change. Aquat. Bot. 118, 24–37. (doi:10.1016/j.aquabot.2014.05.008)
27. Raven JA, Beardall J. 2016 The ins and outs of carbon dioxide. J. Exp. Bot. 67, 1–13. (doi:10.1093/jxb/erv451)
28. Fernández PA, Hurd CL, Roleda MY. 2014 Bicarbonate uptake via an anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. J. Phycol. 50, 998–1008. (doi:10.1111/jpy.12247)
29. Young JN, Heureux AMC, Sharwood RE, Rickaby REM, Morel FMM, Whitney SM. 2016 Large variations in the Rubisco kinetics of diatoms reveals diversity among their carbon concentrating mechanisms. J. Exp. Bot. 67, 3445–3456. (doi:10. 1093/jxb/erw163)
30. Tchernov D, Livne A, Kaplan A, Sukenik A. 2008 The kinetic properties of ribulose-1,5-bisphosphate carboxylase/oxygenase may explain the high apparent photosynthetic affinity of Nannochloropsis sp. to ambient inorganic carbon. Isr. J. Plant Sci. 56, 37–44. (doi:10.1560/IJPS.56.1-2.37)
31. Bhatti S, Colman B. 2008 Inorganic carbon acquisition in some synurophyte algae. Physiol. Plant. 133, 33–40. (doi:10.1111/j.1399-3054.2008. 01061.x)
32. Johnston AM. 1991 The acquisition of inorganic carbon by marine macroalgae. Can. J. Bot. 69, 1123–1132. (doi:10.1139/b91-144)
33. Newman SM, Cattolico RA. 1987 Structural, functional and evolutionary analysis of Ribulose-1,5-bisphosphate carboxylase from the chromophyte alga Olisthodiscus luteus. Plant Physiol. 84, 483–490. (doi:10.1104/pp.84.2.483)
34. Newman SM, Derocher J, Cattolico RA. 1989 Analysis of chromophytic and rhodophytic ribulose-1.5-bisphosphonate carboxylase indicated extensive structural and functional similarities among evolutionarily diverse algae. Plant Physiol. 91, 939–946. (doi:10.1104/pp.91.3.939)
35. Tcherkez GGB, Farquhar GD, Andrews TJ. 2006 Despite slow catalysis and confused kinetics, nearly all ribulose bisphosphate carboxylases may be nearly perfectly optimised. Proc. Natl Acad. Sci. USA 103, 7246–7251. (doi:10.1073/pnas.0600605103)
36. Young JN, Rickaby REM, Kapralov MV, Filatov DA. 2012 Adaptive signals in ancient Rubisco reveal a history of ancient atmospheric carbon dioxide. Phil. Trans. R. Soc. B 367, 483–492. (doi:10.1098/rstb. 2011.0145)
37. Maberly SC. 1996 Diel, episodic and seasonal changes in pH and inorganic carbon in a productive lake. Freshwater Biol. 35, 579–598. (doi:10.1111/j. 1365-2427.1996.tb01770.x)
38. Casper P, Maberly SC, Hall GH, Finlay BJ. 2000 Fluxes of methane and carbon dioxide from a small productive lake to the atmosphere. Biogeochemistry 49, 1–10. (doi:10.1023/A:1006269900174)
39. Saxby-Rouen KJ, Leadbeater BS, Reynolds CS. 1998 The growth of Synura petersenii (Synurophyceae) and components of the dissolved inorganic carbon system. Phycologia 37, 467–477. (doi:10.2216/i0031-8884-37-6-467.1)
40. Bhatti S, Colman B. 2005 Inorganic carbon acquisition in the chrysophyte alga Mallomonas papillosa. Can. J. Bot. 83, 891–897. (doi:10.1139/b05-075)
41. Raven JA, Ball LA, Beardall J, Giordano M, Maberly SC. 2005 Algae lacking carbon-concentrating mechanisms. Can. J. Bot. 83, 879–890. (doi:10. 1139/b05-074)
42. Bhatti S, Colman B. 2011 Evidence of the occurrence of photorespiration in synurophyte algae. Photosynth. Res. 109, 251–256. (doi:10.1007/s11120-011-9639-z)
43. Wilken S, Huisman J, Naus-Wiezer S, van Donk E. 2013 Mixotrophic organisms became more heterotrophic with rising temperatures. Ecol. Lett. 16, 225–233. (doi:10.1111/ele.12033)
44. Yamada K, Yoshikawa S, Inchinomiya M, Kuwata A, Kamiya M, Ohki K. 2014 Effects of silicon-limitation on growth and morphology of Triparma laevis NIES-2565 (Parmales, Heterokontophyta). PLoS ONE 9, e103289. (doi:10.137q/journal.pone. 0103289)
45. Finkel ZV. 2016 Silicification in Microalgae. In The physiology of microalgae. Developments in applied phycology 6 (eds MA Borowitzka, J Beardall, JA Raven), pp. 289–300. Cham, Switzerland: Springer International Publishing.
46. Milligan AJ, Morel FMM. 2002 A proton buffering role for silica in diatoms. Science 297, 1848–1850. (doi:10.1126/science.1074958)
47. Hibberd DJ. 1978 The fine structure of Synura sphagnicola (Korsch.) Korsch (Chrysophyceae). Brit. Phycol. J. 13, 403–412. (doi:10.1080/000716 17800650451)
48. Huertas IE, Colman B, Espie GS. 2002 Mitochondrial-driven bicarbonate transport supports photosynthesis in a marine microalga. Plant Physiol. 130, 284–291. (doi:10.1104/pp.004598)
49. Huertas IE, Colman B, Espie GS. 2002 Inorganic carbon acquisition and its energization in eustimatophyte algae. Funct. Plant. Biol. 29, 271–277. (doi:10.1071/PP01181)
50. 2 -concentrating mechanism in the unicellular alga Eustigmatos vischeri. Eur. J. Phycol. 40, 409–415. (doi:10.1080/09670260500342571)
51. Colman A, Huertas IE, Bhati S, Dason JS. 2002 The diversity of inorganic carbon acquisition mechanisms in eukaryotic algae. Funct. Plant Biol. 29, 261–270. (doi:10.1071/PP01184)
52. Munoz J, Merrett MJ. 1989 Inorganic carbon transport in some marine eukaryotic microalgae. Planta 178, 450–455. (doi:10.1007/BF00963814)
53. Merrett MJ, Nimer MJ, Dong LF. 1996 The ulilization of bicarbonate ions by the marine microalga Nannochloropsis oculata (Droop) Hibberd. Plant Cell Environ. 19, 478–484. (doi:10.1111/j.1365-3040. 1996.tb00340.x)
54. Sukenik A, Tchernov D, Kaplan A, Huertas E, Lubian LM, Livne A. 1997 Uptake, efflux and photosynthetic utilization of inorganic carbon by the eustigmatophyte Nannochloropsis sp. J. Phycol. 33, 969–974. (doi:10.1111/j.0022-3646.1997. 00969.x)
55. 2 evolution during photosynthesis by marine microorganism. Curr. Biol. 7, 723–738. (doi:10. 1016/S0960-9822(06)00330-7)
56. Huertas IE, Lubian LM. 1998 Comparative study of inorganic carbon utilization and photosynthetic responses in Nannochloris (Chlorophyceae) and Nannochloropsis (Eustigmatophyceae) species. Can. J. Bot. 76, 1104–1108. (doi:10.1139/b98-068)
57. 2 efflux in the marine microalgae Nannochloropsis gaditana. Planta 211, 43–49. (doi:10.1007/s004250000254)
58. Hanson DT, Collins AM, Jones HDT, Roesgen J, Lopez-Nieves S, Timlin JA. 2014 On-line stable isotope gas exchange reveals an inducible but leaky carbon concentrating mechanism in Nannochloropsis salina. Photosynth. Res. 121, 311–322. (doi:10. 1007/s11120-014-0001-0)
59. Raso S, van Genugten B, Vermuë M, Wijffels RH. 2012 Effect of oxygen concentration on the growth of Nannochloropsis sp. at low light intensity. J. Appl. Phycol. 24, 863–871. (doi:10.1007/s10811-011-9706-z)
60. Maruyama I, Nakamura T, Matsubayashi T, Ando Y, Maeda T. 1986 Identification of the alga known as ‘marine Chlorella’ as a member of the Eustigmatophyceae. Jap. J. Phycol. 34, 319–325.
61. Hibberd DJ, Leedale GF. 1972 Observations on the cytology and ultrastructure of the new algal class, Eustigmatophyceae. Ann. Bot. 36, 49–71. (doi:10. 1093/oxfordjournals.aob.a084577)
62. Suda S, Atsumi M, Miyashita M. 2002 Taxonomic characterization of a marine Nannochloropsis species N. oceanica sp. nov. (Eustigmatophyceae). Phycologia 4, 273–279. (doi:10.2216/i0031-8884-41-3-273.1)
63. 2 inducible chloroplast envelope protein LIP-36 from Chlamydomonas reinhardtii. Plant Physiol. 114, 265–273. (doi:10.1104/pp.114.1.265)
64. 2 -responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol. 135, 1595–1607. (doi:10.1104/pp.104. 041400)
65. Poliner E et al. 2015 Transcriptional coordination of physiological responses in Nannochloropsis oceanica CCM1779 under light/dark cycles. Plant J. 83, 1097–1113. (doi:10.1111/tpj.12944)
66. 3) transporters. Mol. Aspects Med. 34, 159–182. (doi:10.1016/j.mam.2012.10.008)
67. Raven JA. 1984 Energetics and transport in aquatic plants. New York, NY: A.R. Liss.
68. Raven JA. 2016 Chloride: essential micronutrient and multifunctional beneficial ion. J. Exp. Bot. 68, 359–367. (doi:10.1093/jxb/erw421)
69. Li J, Han D, Wang D, Ning K, Jia J, Jing X, Hunang S, Chen Q, Xu J. 2014 Choreography of transcriptomics and lipidomics of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell 26, 1645–1665. (doi:10. 1105/tpc.113.121418)
70. Maberly SC. 1990 Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J. Phycol. 26, 439–449. (doi:10.1111/j.0022-3646. 1990.00439.x)
71. Raven JA, Beardall J, Roberts S. 1989 The ecophysiology of inorganic carbon assimilation by Durvillaea potatorum (Durvillaeales, Phaeophyta). Phycologia 28, 429–437. (doi:10.2216/i0031-8884-28-4-429.1)
72. Raven JA, Beardall J, Johnston AM, Kübler JE, Geoghegan I. 1995 Inorganic carbon acquisition by Hormosira banksii (Phaeophyta: Fucales) and its epiphyte Notheia anomala (Phaeophyta: Fucales). Phycologia 34, 267–277. (doi:10.2216/i0031-8884-34-4-267.1)
73. Raven JA, Beardall J, Johnston AM, Kübler JE, McInroy SG. 1996 Inorganic carbon acquisition by Xiphophora chondrophylla (Phaeophyta: Fucales). Phycologia 35, 83–89. (doi:10.2216/i0031-8884-35-2-83.1)
74. Zou D, Gao K. 2010 Acquisition of inorganic carbon by Endarachne binghamianum (Scytosiphonales, Phaeophyta). Eur. J. Phycol. 45, 117–126. (doi:10. 1080/09670260903383909)
75. 2 ocean. Glob. Change Biol. 17, 2488–2497. (doi:10.1111/j.1365-2486.2011. 02411.x)
76. 15 N variation in a large collection of macroalgae. J. Phycol. 47, 1023–1035. (doi:10.1111/j.1529-8817.2011.01045.x)
77. Zou D, Gao K, Chen W. 2011 Photosynthetic carbon acquisition in Sargassum henslowianum (Fucales, Phaeophyta), with special reference to the comparison between vegetative and reproductive tissue. Photosynth. Res. 107, 159–168. (doi:10. 1007/s11120-010-9612-2)
78. Fernández PA, Roleda MY, Hurd CL. 2015 Effects of ocean acidification on the photosynthetic performance, carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera. Photosynth. Res. 124, 293–304. (doi:10.1007/s11120-015-0138-5)
79. Middelboe AL, Hansen PJ. 2007 Direct effects of pH and inorganic carbon on macroalgal photosynthesis and growth. Mar. Biol. Res. 3, 134–144. (doi:10. 1080/17451000701320556)
80. Stepien CC. 2015 Impacts of geography, taxonomy and functional group on inorganic carbon use patterns in marine macrophytes. J. Ecol. 103, 1372–1383. (doi:10.1111/1365-2745.12451)
81. Boller AR, Thomas PJ, Cavenaugh M, Scott KM. 2015 Isotopic discrimination and kinetic parameters of Rubisco from the marine bloom forming diatom Skeletonema costatum. Geobiology 13, 33–43. (doi:10.1111/gbi.12112)
82. Johnston AM, Raven J.A. 1986 The utilization of bicarbonate by the macroalga Ascophylum nodosum (L.) Le Jol. Plant Cell Environ. 9, 175–184.
83. Johnston AM, Raven JA. 1986 The analysis of photosynthesis in air and water by the Ascophyllum nodosum (L.) Le Jol. Oeologia 69, 175–184. (doi:10.1007/bf00377636)
84. 4-like characteristics of the intertidal macroalgae Ascophyllum nodosum (L.) Le Jolis (Fucales, Phaeophyta). Phycologia 26, 159–166. (doi:10. 2216/i0031-8884-26-2-159.1)
85. Surif MB, Raven JA. 1989 Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia 78, 97–105. (doi:10.1007/BF00377203)
86. Surif MB, Raven JA. 1990 Photosynthetic gas exchange in eulittoral and normally submersed members of the Fucales and Laminariales: interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82, 68–80. (doi:10.1007/BF00318535)
87. Lüning K. 1990 Seaweeds: their environment, biogeography and physiology. New York, NY: John Wiley.
88. Black CC, Burris JE, Everson RG. 1976 Influence of oxygen concentration of photosynthesis in marine plants. Aust. J. Plant Physiol. 3, 81–86. (doi:10. 1071/PP9760081)
89. 2 evolution in marine plants. Aust. J. Plant Physiol. 3, 73–78. (doi:10.1071/PP9760073)
90. Burris JE. 1977 Photosynthesis, photorespiration, and dark respiration in eight species of algae. Mar. Biol. 39, 371–379. (doi:10.1007/BF00391940)
91. Dromgoole FI. 1978 The effects of pH and inorganic carbon on photosynthesis and dark respiration of Carpophyllum (Fucales, Phaeophyceae). Aquat. Bot. 4, 11–22. (doi:10.1016/0304-3770(78)90003-7)
92. 2 on dark respiration and apparent photosynthesis of marine macro-algae. Aquat. Bot. 4, 281–297. (doi:10.1016/0304-3770(78)90025-6)
93. Gross W. 1990 Occurrence of glycolate oxidase and hydroxypyruvate reductase in Egregia menziesii (Phaeophyta). J. Phycol. 26, 381–383. (doi:10. 1111/j.0022-3646.1990.00381.x)
94. Iwamoto K, Ikawa T. 1997 Glycolate metabolism and subcellular distribution of glycolate oxidase in Spatoglossum pacificum (Phaeophyceae, Chromophyta). Phycol. Res. 45. 77–83. (doi:10. 1111/j.1440-1835.1997.tb00066.x)
95. Raven JA, Hurd CL. 2012 Ecophysiology of photosynthesis in macroalgae. Photosynth. Res. 113, 105–125. (doi:10.1007/s11120-012-9768-z)
96. Zhang X, Hu H, Tan T. 2006 Photosynthetic organic carbon utilization by gametophytes and sporophytes of Undaria pinnatifida (Phaeophyceae). Phycologia 45, 642–647. (doi:10.2216/05-28.1)
97. Larsson C, Axelsson L. 1999 Bicarbonate uptake and utilization in marine macroalgae. Eur. J. Phycol. 34, 79–86. (doi:10.1080/09670269910001736112)
98. Schmid R. 1998 Photosynthesis by Ectocarpus siliculosus in red light and after pulses of blue light at high pH—evidence for bicarbonate uptake. Plant Cell Environ. 21, 523–529. (doi:10.1046/j.1365-3040.1998.00297.x)
99. 2 dependence of photosynthesis. Planta 187, 60–66. (doi:10.1007/BF00201624)
100. Schmid R, Hillrichs S. 2001 Uptake and accumulation of inorganic carbon in Ectocarpus sliculosus and its relation to blue light stimulation of photosynthesis. Eur. J. Phycol. 36, 257–264. (doi:10.1080/09670260110001735408)
101. Walker NA, Smith FA, Cathers IR. 1980 Bicarbonate assimilation by fresh-water charophytes and higher plants: I. Membrane transport of bicarbonate is not proven. J. Membr. Biol. 57, 51–58. (doi:10.1007/BF01868985)
102. Price GD, Badger MR, Bassett ME, Whitecross MI. 1985 Involvement of plasmalemmasomes and carbonic anhydrase in photosynthetic utilization of bicarbonate in Chara corallina. Aust. J. Plant Biol. 12, 241–256. (doi:10.1071/PP9850241)
103. Price GD, Badger MR. 1985 Inhibition by proton buffers of photosynthetic utilization of bicarbonate in Chara corallina. Aust. J. Plant Biol. 12, 257–267. (doi:10.1071/PP9850257)
104. Schmid R, Dring MJ. 1993 Rapid, blue light-induced acidifications at the surface of Ectocarpus and other marine macroalgae. Plant Physiol. 101, 907–913. (doi:10.1104/pp.101.3.907)
105. 3 at high pH by the brown macroalga Laminaria saccharina. Eur. J. Phycol. 35, 53–59. (doi:10.1080/09670260010001735621)
106. Klenell M, Snoejis P, Pedersén M. 2004 Active carbon uptake in Laminaria digitata and L. saccharina (Phaeophyta) is driven by a proton pump in the plasma membrane. Hydrobiologia 514, 41–53. (doi:10.1023/B:hydr.0000018205.80186.3e)
107. 2 concentrating mechanism in Laminaria saccharina. Photosynth. Res. 88, 259–268. (doi:10. 1007/s11120-006-9039-y)
108. Giordano M, Maberly SC. 1989 Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81, 534–539. (doi:10.1007/BF00378965)
109. Haglund K, Ramazanov Z, Mtolera M, Pedersén M. 1992 Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L. and Laminaria saccharina (L.) Lamour. (Phaeophyta). Planta 188, 1–6. (doi:10.1007/BF01160705)
110. Silberfeld T, Leigh JW, Verbruggen H, Cruaud C, De Reviers B. 2010 A multilocus time-calibrated phylogeny of the brown algae (Heterokonotophyta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the ‘brown algal crown radiation’. Mol. Phylogenet. Evol. 56, 659–674. (doi:10.1016/j.ympev.2010.04.020)
111. Silberfeld T, Racault M-FLP, Fletcher RL, Couloux A, Rousseau F, de Reviers B. 2011 Systematics and evolutionary history of pyrenoid-bearing taxa in the brown algae (Phaeophyceae). Eur. J. Phycol. 46, 361–377. (doi:10.1080/09670262.2011. 628698)
112. Gravot A, Dittami SM, Rousvoal S, Lugan R, Eggert A, Collén J, Boyen C, Bouchereau A, Tonon T. 2010 Diurnal oscillations of metabolite abundances and gene analysis prove new insights into central carbon metabolic processes of the brown alga Ecocarpus siliculosus. New Phytol. 188, 98–110. (doi:10.1111/j.1469-8137.2010.03400.x)
113. 2 -concentrating mechanisms: lessons for the future. J. Exp. Bot. 64, 769–786. (doi:10. 1093/jxb/ers390)
114. Ye N et al. 2015 Saccharina genomes provide novel insights into kelp biology. Nat. Commun. 6, 6986. (doi:10.1038/ncomms7986)
115. Bi Y, Zhou Z. 2016 Absorption and transport of inorganic carbon in kelps with emphasis on Saccharina japonica. In Applied photosynthesis— new progress (ed. MM Najafpour), pp. 111–131. Rijeka, Croatia: InTech Open Publishers.
116. Newman S, Deracher TS, Cattolico RA. 1989 Analysis of chromophytic and rhodophyte ribulose-1,5-bisphosphate indicates extensive structural and functional similarities among evolutionarily diverse algae. Plant Physiol. 91, 939–946. (doi:10.1104/pp. 91.3.939)
117. Clark DR, Flynn KJ. 2000 The relationship between dissolved inorganic carbon concentration and growth rate in marine phytoplankton. Proc. R. Soc. B. 267, 953–959. (doi:10.1098/rspb.2000.1096)
118. Nimer NA, Iglesias-Rodriguez MD, Merrett MJ. 1997 Bicarbonate utilization by marine phytoplankton species. J. Phycol. 33, 625–631. (doi:10.1111/j. 0022-3646.1997.00625.x)
119. Yamaguchi H, Nakayama T, Murakami A, Inouye I. 2010 Phylogeny and taxonomy of the Raphidophyceae (Heterokontophyta) and Chlorinolomas sublosa gen. et sp. nov., a new marine sand-dwelling raphidophyte. J. Plant Res. 123, 333–342. (doi:10.1007/s10265-009-0281-1)
120. 2 concentrating mechanism in Botrydiopsis (Tribophyceae). Phycologia 23, 511–513. (doi:10. 2216/i0031-8884-23-4-511.1)
121. Ichinomiya M et al. 2016 Diversity and oceanic distribution of the Parmales (Bolidiphyceae), a picoplanktonic group closely related to the diatoms. ISME J. 10, 2419–2434. (doi:10.1038/ismej.2016. 38)
122. DeYoe HR, Stockwell DA, Bidigare RR, Latasa M, Johnston PW, Hargreaves PE, Suttle CA. 1997 Description and characterization of the algal species Aureoumbra lagunensis gen. et sp. nov, and referral of Aureoumbra and Aureococcus to the Pelagophyceae. J. Phycol. 33, 1042–1048. (doi:10. 1111/j.0022-3646.1997.01042.x)
123. 4 pathway? Planta 133, 191–196. (doi:10. 1007/BF00391918)
124. Kremer BP. 1980 Taxonomic implications of algal photoassimilate patterns. Brit. Phycol. J. 15, 399–409. (doi:10.1080/00071618000650401)
125. Kremer BP. 1980 Photorespiration and β-carboxylation in brown macroalgae. Planta 150, 189–190. (doi:10.1007/BF00582365)
126. Busch S, Schmid R. 2001 Enzymes associated with β-carboxylation in Ectocarpus siliculosus (Phaeophyceae): are they involved in net carbon acquisition? Eur. J. Phycol. 36, 61–70. (doi:10. 1017/s0967026201003067)
127. Hillrichs S, Schmid R. 2001 Activation by blue light of inorganic carbon acquisition for photosynthesis in Ectocarpus siliculosus: organic acid pools and short-term carbon fixation. Eur. J. Phycol. 36, 71–79. (doi:10.1080/09670260110001735218)
128. Koch M, Bowes G, Ross C, Zhang X-H. 2013 Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Chang. Biol. 19, 103–132. (doi:10.1111/j.1365-2486.2012. 02791.x)
129. 4 -metabolism in marine brown macrophytic algae. Z. Naturforsch. 39C, 840–847.
130. Küppers U, Kremer BP. 1978 Longitudinal profiles of carbon dioxide fixation capacities in marine macroalgae. Plant Physiol. 62, 49–53. (doi:10. 1104/pp.62.1.49)
131. Axelsson L, Carlberg S, Ryberg H. 1989 Adaptations by macroalgae to low carbon availability. I. A buffer system in Ascophyllum nodosum, associated with photosynthesis. Plant Cell Environ. 12, 765–770. (doi:10.1111/j.1365-3040.1989.tb01637.x)
132. Axelsson L, Carlberg S, Ryberg H. 1989 Adaptations by macroalgae to low carbon availability. II. Ultrastructural specializations, related to the function of a photosynthetic buffer system in the Fucaceae. Plant Cell Environ. 12, 771–778. (doi:10. 1111/j.1365-3040.1989.tb01638.x)
133. Forster RM, Dring MJ. 1994 Influence of blue light on the photosynthetic capacity of marine plants from different taxonomic, ecological and morphological groups. Eur. J. Phycol. 29, 21–27. (doi:10.1080/09670269400650441)
134. Dring MJ, Forster RM, Schmid R. 1994 Ecological significance of blue light stimulation of photosynthetic capacity in Laminaria spp. and other brown algae. Mar. Ecol. Progr. Ser. 113, 271–277. (doi:10.3354/meps113271)
135. Kawamatsu Y, Boyer JS. 1999 Photosynthesis and carbon storage between tides in a brown alga, Fucus vesiculosus. Mar. Biol. 133, 361–369. (doi:10. 1007/s002270050475)
136. Keeley JE. 1998 CAM photosynthesis in submerged aquatic plants. Bot. Rev. 64, 121–175. (doi:10. 1007/BF02856581)
137. 4 pathway. J. Exp. Bot. 62, 3049–3059. (doi:10.1093/jxb/err012)
138. 4 -related genes. PLoS ONE 9, e110154. (doi:10.1371/journal.pone.0110154)
139. Kroth PG et al. 2008 A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from whole genome analysis. PLoS ONE 3, e1426. (doi:10.1371/journal.pone. 0001426)
140. Descolas-Gros C, Oriol L. 1992 Variations in carboxylase activity in marine phytoplankton cultures. Mar. Ecol. Progr. Ser. 85, 163–169. (doi:10.3354/meps085163)
141. Wurch LL, Bertrand EH, Saito MA, van Mooy BAS, Dyhrman ST. 2011 Proteome changes driven by phosphorus deficiency in the brown tide-forming alga Aureococcus anophagefferens. PLoS ONE 6, e28949. (doi:10.1371/journal.pone. 0028949)