Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP24058
RESEARCH ARTICLE
Contents Vol 51(7)

Acclimation mechanism of microalgal photosynthetic apparatus under low atmospheric pressures – new astrobiological perspectives in a Mars-like atmosphere

Charalampia-Stavroula Gritsi A , Evangelos Sarmas A , Vangelis Daskalakis https://orcid.org/0000-0001-8870-0850 B and Kiriakos Kotzabasis https://orcid.org/0000-0002-1002-6365 A *
+ Author Affiliations
- Author Affiliations

A Department of Biology, University of Crete, Voutes University Campus, Heraklion, Crete GR 70013, Greece.

B Department of Chemical Engineering, School of Engineering, University of Patras, Patras GR 26504, Greece.

* Correspondence to: kotzab@uoc.gr

Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 51, FP24058 https://doi.org/10.1071/FP24058
Submitted: 8 March 2024  Accepted: 25 May 2024  Published: 20 June 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

This study reveals a new acclimation mechanism of the eukaryotic unicellular green alga Chlorella vulgaris in terms of the effect of varying atmospheric pressures on the structure and function of its photosynthetic apparatus using fluorescence induction measurements (JIP-test). The results indicate that low (400 mbar) and extreme low (<10 mbar) atmospheric pressure decreases the density and thus increases the fluidity of the thylakoid membrane, possibly facilitating plastoquinone (PQ) movement within the membrane and resulting in enhanced photosynthetic electron flow and photochemical quenching. Molecular dynamic simulations of different light harvesting complexes within thylakoid membrane models confirm this mechanism and reveal the associated atomic scale details. The exposure of microalga to an extremely low pressure (<10 mbar) in a 100% CO2 atmosphere (simulating the Mars atmosphere), reveals that the impact of extremely low atmospheric pressure on PQ mobility within the photosynthetic membrane, coupled with the low density of an almost 100% CO2 Mars-like atmosphere, results to a similar photosynthetic efficiency to that on Earth. These findings pave the way for the identification of novel functional acclimation mechanisms of microalgae to extreme environments that are vastly distinct from those found on Earth.

Keywords: acclimation, astrobiology, atmospheric composition, atmospheric pressure, extremophiles, microalgae, molecular dynamics, photosynthesis.

References

Amesz J (1973) The function of plastoquinone in photosynthetic electron transport. Biochimica et Biophysica Acta (BBA) – Reviews on Bioenergetics 301, 35-51.
| Crossref | Google Scholar | PubMed |

Battistuzzi M, Cocola L, Salasnich B, Erculiani MS, Alei E, Morosinotto T, Claudi R, Poletto L, La Rocca N (2020) A new remote sensing-based system for the monitoring and analysis of growth and gas exchange rates of photosynthetic microorganisms under simulated non-terrestrial conditions. Frontiers in Plant Science 11, 182.
| Crossref | Google Scholar | PubMed |

Berendsen HJC, van der Spoel D, van Drunen R (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Computer Physics Communications 91(1), 43-56.
| Crossref | Google Scholar |

Bernetti M, Bussi G (2020) Pressure control using stochastic cell rescaling. The Journal of Chemical Physics 153(11), 114107.
| Crossref | Google Scholar | PubMed |

Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. The Journal of Chemical Physics 126(1), 014101.
| Crossref | Google Scholar |

Chrysafoudi A, Maity S, Kleinekathöfer U, Daskalakis V (2021) Robust strategy for photoprotection in the light-harvesting antenna of diatoms: a molecular dynamics study. The Journal of Physical Chemistry Letters 12(39), 9626-9633.
| Crossref | Google Scholar | PubMed |

Cycil LM, Hausrath EM, Ming DW, Adcock CT, Raymond J, Remias D, Ruemmele WP (2021) Investigating the growth of algae under low atmospheric pressures for potential food and oxygen production on mars. Frontiers in Microbiology 12, 733244.
| Crossref | Google Scholar | PubMed |

Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an N·log (N) method for Ewald sums in large systems. The Journal of Chemical Physics 98(12), 10089-10092.
| Crossref | Google Scholar |

Daskalakis V, Maity S, Hart CL, Stergiannakos T, Duffy CDP, Kleinekathöfer U (2019) Structural basis for allosteric regulation in the major antenna trimer of photosystem II. The Journal of Physical Chemistry B 123(45), 9609-9615.
| Crossref | Google Scholar | PubMed |

Daskalakis V, Papadatos S, Stergiannakos T (2020) The conformational phase space of the photoprotective switch in the major light harvesting complex II. Chemical Communications 56(76), 11215-11218.
| Crossref | Google Scholar | PubMed |

Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1767(4), 272-280.
| Crossref | Google Scholar | PubMed |

Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, Tyryshkin A (2001) The origin of atmospheric oxygen on earth: the innovation of oxygenic photosynthesis. Proceedings of the National Academy of Sciences 98, 2170-2175.
| Crossref | Google Scholar |

Escobar CM, Nabity JA (2017) Past, present, and future of closed human life support. In ‘47th International Conference on Environmental Systems. 16–20 July 2017, Charleston, South Carolina’. (Texas Tech University Libraries: USA)

Fischer WW, Hemp J, Johnson JE (2016) Evolution of oxygenic photosynthesis. Annual Review of Earth and Planetary Sciences 44, 647-683.
| Crossref | Google Scholar |

Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. Journal of Computational Chemistry 18(12), 1463-1472.
| Crossref | Google Scholar |

Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428(6980), 287-292.
| Crossref | Google Scholar | PubMed |

Maity S, Gelessus A, Daskalakis V, Kleinekathöfer U (2019) On a chlorophyll-caroteinoid coupling in LHCII. Chemical Physics 526, 110439.
| Crossref | Google Scholar |

Mountourakis F, Papazi A, Kotzabasis K (2021) The microalga Chlorella vulgaris as a natural bioenergetic system for effective CO2 mitigation—new perspectives against global warming. Symmetry 13, 997.
| Crossref | Google Scholar |

Mountourakis F, Papazi A, Maragkoudakis A, Stamatis N, Kotzabasis K (2023) Evidence of physiological adaptation of Chlorella vulgaris under extreme salinity – new insights into a potential halotolerance strategy. Environmental and Experimental Botany 216, 105543.
| Crossref | Google Scholar |

Murukesan G, Leino H, Mäenpää P, Ståhle K, Raksajit W, Lehto HJ, Allahverdiyeva-Rinne Y, Lehto K (2016) Pressurized martian-like pure CO2 atmosphere supports strong growth of cyanobacteria, and causes significant changes in their metabolism. Origins of Life and Evolution of Biospheres 46(1), 119-131.
| Crossref | Google Scholar |

Navakoudis E, Stergiannakos T, Daskalakis V (2022) A perspective on the major light-harvesting complex dynamics under the effect of pH, salts, and the photoprotective PsbS protein. Photosynthesis Research 156, 163-177.
| Crossref | Google Scholar | PubMed |

Paynea RC, Brownleeb D, Kastinga JF (2020) Oxidized micrometeorites suggest either high pCO2 or low pN2 during the Neoarchean. Proceedings of the National Academy of Sciences 117, 1360-1366.
| Crossref | Google Scholar |

Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397, 625-628.
| Crossref | Google Scholar |

Prandi IG, Viani L, Andreussi O, Mennucci B (2016) Combining classical molecular dynamics and quantum mechanical methods for the description of electronic excitations: the case of carotenoids. Journal of Computational Chemistry 37(11), 981-991.
| Crossref | Google Scholar | PubMed |

Retegan M, Pantazis DA (2017) Differences in the active site of water oxidation among photosynthetic organisms. Journal of the American Chemical Society 139(41), 14340-14343.
| Crossref | Google Scholar | PubMed |

Revellame ED, Aguda R, Chistoserdov A, Fortela DL, Hernandez RA, Zappi ME (2021) Microalgae cultivation for space exploration: assessing the potential for a new generation of waste to human life-support system for long duration space travel and planetary human habitation. Algal Research 55, 102258.
| Crossref | Google Scholar |

Ru ITK, Sung YY, Jusoh M, Wahid MEA, Nagappan T (2020) Chlorella vulgaris: a perspective on its potential for combining high biomass with high value bioproducts. Applied Phycology 1, 2-11.
| Crossref | Google Scholar |

Ruan M, Li H, Zhang Y, Zhao R, Zhang J, Wang Y, Gao J, Wang Z, Wang Y, Sun D, Ding W, Weng Y (2023) Cryo-EM structures of LHCII in photo-active and photo-protecting states reveal allosteric regulation of light harvesting and excess energy dissipation. Nature Plants 9(9), 1547-1557.
| Crossref | Google Scholar | PubMed |

Ruban AV (2018) Light harvesting control in plants. FEBS Letters 592(18), 3030-3039.
| Crossref | Google Scholar | PubMed |

Seiwert D, Witt H, Janshoff A, Paulsen H (2017) The non-bilayer lipid MGDG stabilizes the major light-harvesting complex (LHCII) against unfolding. Scientific Reports 7, 5158.
| Crossref | Google Scholar | PubMed |

Senger H, Brinkmann G (1986) Protochlorophyll(ide) accumulation and degradation in the dark and photoconversion to chlorophyll in the light in pigment mutant C-2A’ of Scenedesmus obliquus. Physiologia Plantarum 68, 119-124.
| Crossref | Google Scholar |

Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. In ‘Photosynthesis: from light to biosphere’. (Ed. P Mathis) pp. 977–980. (Kluwer Academic Publishers: Dordrecht, Netherlands)

Tsimilli-Michael M (2020) Special issue in honour of Prof. Reto J. Strasser – Revisiting JIP-test: an educative review on concepts, assumptions, approximations, definitions and terminology. Photosynthetica 58, 275-292.
| Crossref | Google Scholar |

van Eerden FJ, de Jong DH, de Vries AH, Wassenaar TA, Marrink SJ (2015) Characterization of thylakoid lipid membranes from cyanobacteria and higher plants by molecular dynamics simulations. Biochimica et Biophysica Acta (BBA) – Biomembranes 1848(6), 1319-1330.
| Crossref | Google Scholar | PubMed |

Verseux C, Heinicke C, Ramalho TP, Determann J, Duckhorn M, Smagin M, Avila M (2021) A low-pressure, N2/CO2 atmosphere is suitable for cyanobacterium-based life-support systems on Mars. Frontiers in Microbiology 12, 611798.
| Crossref | Google Scholar | PubMed |

Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. Journal of Computational Chemistry 25(9), 1157-1174.
| Crossref | Google Scholar | PubMed |

Wang W, Yu L-J, Xu C, Tomizaki T, Zhao S, Umena Y, Chen X, Qin X, Xin Y, Suga M, Han G, Kuang T, Shen J-R (2019) Structural basis for blue-green light harvesting and energy dissipation in diatoms. Science 363(6427), eaav0365.
| Crossref | Google Scholar |

Wong Y (2017) Growth medium screening for Chlorella vulgaris growth and lipid production. Journal of Aquaculture & Marine Biology 6, 00143.
| Crossref | Google Scholar |

Zerveas S, Kydonakis E, Moutidis P, Maragkoudakis A, Kotzabasis K (2021) Microalgae strategy in anoxic atmospheres with various CO2 concentrations – environmental and (astro)biotechnological perspectives. Environmental and Experimental Botany 187, 104474.
| Crossref | Google Scholar |

Zhang L, Silva D-A, Yan YJ, Huang X (2012) Force field development for cofactors in the photosystem II. Journal of Computational Chemistry 33(25), 1969-1980.
| Crossref | Google Scholar | PubMed |