Versatility of the green microalga cell vacuole function as revealed by analytical transmission electron microscopy.
Vacuole is a multifunctional compartment central to a large number of functions (storage, catabolism, maintenance of the cell homeostasis) in oxygenic phototrophs including microalgae. Still, microalgal cell vacuole is much less studied than that of higher plants although knowledge of the vacuolar structure and function is essential for understanding physiology of nutrition and stress tolerance of microalgae. Here, we combined the advanced analytical and conventional transmission electron microscopy methods to obtain semi-quantitative, spatially resolved at the subcellular level information on elemental composition of the cell vacuoles in several free-living and symbiotic chlorophytes. We obtained a detailed record of the changes in cell and vacuolar ultrastructure in response to environmental stimuli under diverse conditions. We suggested that the vacuolar inclusions could be divided into responsible for storage of phosphorus (mainly in form of polyphosphate) and those accommodating non-protein nitrogen (presumably polyamine) reserves, respectively.The ultrastructural findings, together with the data on elemental composition of different cell compartments, allowed us to speculate on the role of the vacuolar membrane in the biosynthesis and sequestration of polyphosphate. We also describe the ultrastructural evidence of possible involvement of the tonoplast in the membrane lipid turnover and exchange of energy and metabolites between chloroplasts and mitochondria. These processes might play a significant role in acclimation in different stresses including nitrogen starvation and extremely high level of CO2and might also be of importance for microalgal biotechnology. Advantages and limitations of application of analytical electron microscopy to biosamples such as microalgal cells are discussed.
Lomonosov Moscow State University, Moscow, Russia.
Anastasia
A
Shebanova
Lomonosov Moscow State University, Moscow, Russia.
Tatiana
T
Ismagulova
Lomonosov Moscow State University, Moscow, Russia. solovchenko@mail.bio.msu.ru.|Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Moscow, Russia. solovchenko@mail.bio.msu.ru.|Faculty of Biology, Moscow State University, Leninskie Gori 1/12, 119234, GSP-1 Moscow, Russia. solovchenko@mail.bio.msu.ru.
Alexei
http://orcid.org/0000-0001-6746-8511
A
Solovchenko
Lomonosov Moscow State University, Moscow, Russia.
Olga
O
Baulina
Lomonosov Moscow State University, Moscow, Russia.
Elena
E
Lobakova
Komarov Botanical Institute, Russian Academy of Sciences, St. Petersburg, Russia.|St. Petersburg State University, St. Petersburg, Russia.
Alexandra
A
Ivanova
Lomonosov Moscow State University, Moscow, Russia.
Andrey
A
Moiseenko
Lomonosov Moscow State University, Moscow, Russia.
Konstantin
K
Shaitan
Faculty of fundamental medicine, Lomonosov Moscow State University, Moscow, Russia.
Vladimir
V
Polshakov
Institute of Bio- and Geosciences / Plant Sciences (IBG-2), Forschungszentrum Jülich, Jülich, Germany.
Ladislav
L
Nedbal
Lomonosov Moscow State University, Moscow, Russia.
Olga
O
Gorelova
D002468:Cell Physiological Phenomena; D000460:Chlorophyta / Q000378:metabolism* / Q000502:physiology; D002736:Chloroplasts / Q000378:metabolism; D002479:Inclusion Bodies / Q000378:metabolism; D009682:Magnetic Resonance Spectroscopy; D058086:Microalgae / Q000378:metabolism* / Q000502:physiology; D046529:Microscopy, Electron, Transmission; D014617:Vacuoles / Q000378:metabolism* / Q000648:ultrastructure*
Analytical electron microscopy; Microalgae; Nitrogen; Phosphorus; Polyphosphate; Stress responses; Vacuole
J Microsc. 2008 Aug;231(2):201-14
18778418
Chem Rev. 2008 Nov;108(11):4694-715
18975924
FEMS Microbiol Ecol. 2016 Apr;92 (4):fiw031
26880784
Biol Cell. 2011 Sep;103(9):405-20
21812762
Biotechnol Adv. 2016 Sep-Oct;34(5):550-564
26795876
EMBO J. 1989 Oct;8(10 ):2835-41
2479537
J Microsc. 2016 Feb;261(2):177-84
26301324
MRS Bull. 2012 Jan;37(1):53-62
23049161
Biotechnol Adv. 2012 May-Jun;30(3):673-90
22166620
Plant J. 2009 Dec;60(5):882-93
19709388
J Ind Microbiol Biotechnol. 2011 Dec;38(12):1879-90
21882013
Prog Histochem Cytochem. 2004;39(4):185-319
15622702
Science. 2009 Apr 24;324(5926):513-6
19390046
J Bacteriol. 1976 May;126(2):937-50
4437
Sci Rep. 2016 May 16;6:25731
27180903
Arch Microbiol. 2015 Mar;197(2):181-95
25239707
Water Res. 2009 Sep;43(17):4207-13
19616819
Environ Sci Technol. 2013 Oct 15;47(20):11378-9
24093750
Plant Physiol. 1982 Jan;69(1):98-102
16662193
Nat Commun. 2016 Apr 14;7:11228
27075521
Protoplasma. 2010 Jul;243(1-4):25-38
19340523
J Cell Sci. 2003 Mar 15;116(Pt 6):1107-15
12584253
EMBO J. 2002 Feb 1;21(3):259-69
11823419
Planta. 2008 Aug;228(3):367-81
18594857
J Cell Biol. 1963 Apr;17:208-12
13986422
Int Rev Cytol. 2007;264:1-24
17964920
Micron. 2006;37(5):452-8
16376553
Protoplasma. 2001;218(3-4):144-53
11770431
Eur J Histochem. 2013 Nov 05;57(4):e34
24441187
Planta. 2000 May;210(6):897-905
10872220
Plant Physiol. 1991 Nov;97(3):1234-40
16668514
Protoplasma. 2015 Mar;252(2):489-503
25189657
Plant Physiol. 1991 Nov;97(3):1226-33
16668513
Mar Biotechnol (NY). 2014 Oct;16(5):495-501
24807746
Aquat Toxicol. 2013 Sep 15;140-141:324-36
23891781
Curr Opin Cell Biol. 2016 Aug;41:66-72
27125677
Nat Rev Microbiol. 2005 Mar;3(3):251-61
15738951
Protoplasma. 2010 Mar;239(1-4):49-56
19902325
Plant Physiol. 1991 Nov;97(3):1241-8
16668515
Arch Environ Contam Toxicol. 1997 Aug;33(2):156-61
9294243
J Biol Chem. 2001 Dec 7;276(49):46196-203
11579086
Bioresour Technol. 2011 Jan;102(1):17-25
20594826
Plant Cell. 1999 Apr;11(4):587-600
10213780
Biomacromolecules. 2007 Sep;8(9):2675-83
17713945
Plant Physiol. 1995 Dec;109(4):1317-1326
12228672
Biochemistry (Mosc). 2000 Mar;65(3):280-95
10739470
J Cell Sci. 2014 Dec 1;127(Pt 23):5093-104
25315834
Biomed Res Int. 2015;2015:519769
26167488
FEMS Microbiol Ecol. 2003 May 1;44(2):253-9
19719642
Biochim Biophys Acta. 2000 May 1;1465(1-2):37-51
10748246