|
Victor E.
Semenenko is known in
Russia
and in other countries as a contributor to the studies of self-regulation of
physiological functions in photosynthetic cells. He was also the founder of
algal biotechnology in
Russia.
His first
student scientific paper "On the effect of light starvation on the
chloroplasts in leaves of green plants," in which a young researcher
observed the disintegration and division of chloroplasts of the algaSelagenella, was published in 19521. After graduation from the
University of
Kiev
(
Ukraine), V.E. Semenenko
started his research at the
Institute
of
Plant Physiology (
Moscow) under supervision of Professor
Nichiporovich. Since that time his research activities were tightly linked with
the name of this institution. Research and communication with A. Nichiporovich
had a strong influence on the development of basic biological views, and the
personality of Victor Semenenko. His PhD thesis was devoted to the study of
photosynthetic gas exchange processes. In that work he first discovered the
phenomenon light-dependent emission of CO2. The biochemical studies of this
phenomenon in other laboratories had later led to the discovery of
photorespiration2.
After
finishing his PhD thesis in 1958, Victor Semenenko became a leader of a group
associated with the Laboratory of photosynthesis. The group was focused on the
problem of application of the unicellular phototrophic microorganisms in closed
biological for life support systems. The organization of this group, was
prompted by the successful beginning of space exploration in those years and
the emergence of a new branch of knowledge - Space Biology.
Great
success in space exploration in the late 50s and 60s of the XX century gave
rise to the optimism, and enthusiasm in scientific community. Even before
Gagarin's flight into space, the prospects for long-term space travel,
construction of the habitable extraterrestrial stations and orbital complexes
had been discussed. Intensively grown algae have been considered as one of the
main elements of such stations responsible for the biological life support in
space. At that time Victor Semenenko became the head of the Laboratory for
algological studies.
First of
all, the viability and the level of mutations in Chlorella cells during space
flight were studied in 1958. The experiments were conducted on unpiloted
satellites. The results did not demonstrate any significant changes in
physiological states in populations of algae in the flight experiments3.
Another
important step was to examine the compatibility of green unicellular algae and
humans in their permanent contact. This problem was solved in the early 60s in
the joint experiments with the
Institute
of
Biophysics, Medical
Academy of Sciences. A prolonged stay of astronauts in an isolated hermetic cabin,
which was connected to the system of gas exchange ran by a photobioreactor with
unicellular algae, did not affect the status of the crew and as well as the
viability of microalgae4-6.
At the same
time, the selection of the most promising forms of life support systems for
unicellular algae was conducted that implied optimization of their growth in
newly developed closed photobioreactors of various types. As a result, during a
1.5-month continuous experiment, the productivity of Chlorella reached 25-
30 liters of oxygen from
1 liter of cell suspension
per day. These experiments lead to construction of flat-panel photobioreactors,
the reactors with air lifts, turbosorbers, the spray systems for suspension, to
the design of distribution of light energy in a suspension with fiber optics7.
The
principal condition that determined the possibility of the use of biological
life support systems based on algae was high reliability and stability of a
system at the level of algae themselves. In 1967, Victor Semenenko together
with Lev Tsoglin proposed the autoselection theory for populations of
microalgae, which was experimentally verified in 1969-72. This theory
eliminated the possibility of deterioration in gas exchange characteristics of
the unit. It demonstrated the exclusive ability to improve photosynthetic
characteristics and production rates of algae in the course of their long-term
continuous cultivation8,9.
Along with
the regeneration of the atmosphere, the problem of biological life support
system includes the nutrition for the crew - fitness of the biochemical
composition of microalgae to the diet ration of human. The regulation of
biochemical pathways of the photosynthetic metabolism in microalgae became the
major focus of research of Victor Semenenko. Studies in this field had finally
resulted in the hypothesis of endogenous regulation of photosynthesis10. These
studies led to the selection of algal strains - producers of various compounds
and to the development of methods of controlled biosynthesis, which allowed the
maintenance of biochemical composition of microalgae under various extreme
conditions10-12. The two-phase method for cultivation of algae developed in the
70's, made it possible to perform continuous growth of biomass with a
determined biochemical composition without reduction in the photosynthetic
activity13-15.
The studies
of Victor Semenenko in space biology have laid important foundations of modern
biotechnology of microalgae and initiated its development in
Russia.
The wide
spectrum of scientific interests of Victor Semenenko allowed him to go beyond
the practical space biology. In 1971, his group was transformed into a
Laboratory of molecular bases of intracellular regulation, and then into the
Department of Intracellular regulation and biotechnology of photoautotrophic
biosynthesis.
All these
years, microalgae served to Victor Semenenko as an excellent model for
investigation of the principles of self-regulation by virtue of extremely high
plasticity of their metabolism16,17. Together with his wife and colleague, Maya
G. Vladimirova, he founded The Collection of Microalgae (IPPAS), which became a
member of the International Association of Collections. Currently, this is the
most representative collection of microalgae in
Russia.
The main
interests of Viktor Semenenko, as he formulated them, have been focused on
self-regulation of physiological processes and metabolism of photoautotrophic
cells:
-
Elucidation of the physiological responses of the genetic systems of plant
cells.
- Investigation
of molecular and cellular mechanisms of organization of endogenous regulation
of photosynthesis10,18-22.
-
Investigation of metabolism and cell cycle of unicellular photoautotrophic
organism9,23-26.
Along this
way, the most significant discoveries had been made that leaved the unique and
bright mark in science. Among Russian scientists of the 20th century, who made
a significant contribution to the study of the primary processes of
photosynthesis (V.B. Evstigneev, A.A. Krasnovskii), the structure and
biosynthesis of chlorophyll (T. Godnev, A. Shlyk), photosynthetic carbon
metabolism (A.T. Mokronosov, N.G. Doman, E.N. Kondratyev, A.K. Romanova), the
genome of the photosynthetic apparatus (N.M. Sissakian) and photosynthetic
productivity (A.A. Nichiporovich), Victor Semenenko holds a special position.
In the
early 70's Victor Semenenko turned to the old problem of plant Physiol. on the
influence of assimilates (or overfeeding of plants) on photosynthesis in order
to uncover the molecular level of these events. To investigate the metabolic
regulation of photosynthesis three main questions have been asked: 1) what is
the possible nature of the regulatory metabolite or effector; 2) what is the
molecular mechanism of its action in the chloroplast; and 3) what is the
mechanism of coupling of photo- and metabolic regulation?
Screening
among the metabolites, products of photosynthesis, the modified glucose
molecules have been used possess biological function, but are limited in
utilization. One of such molecules was 2-deoxy-D-glucose (2dDG), which was
applied in the studies of the repression of photosynthesis and protein
synthesis in the chloroplast. Further detection of light-dependent repressive
action of 2dDG revealed close cooperation of metabolic regulation and light
regulation in chloroplasts10,19,20,22,27-29,29-37.
In 1982,
the inhibitory analysis and chronology of events in chloroplasts revealed that
the regulatory effect of glucose is carried out at the level of transcription
in chloroplasts22. Later, these findings were confirmed by investigation the transcription
of genes for the proteins of the reaction center of photosystem II. Mutagenesis
of Chlorella vulgaris led to the production of the regulatory mutants, which
were characterized by overproduction of the end-products of
photosynthesis32,38,39. Similar studies had been conducted with cells of the
cyanobacterium Synechocystis sp. PCC 6803, from which the 2dDG-resistant
mutants have been selected40,41. These approaches (M.V. Zvereva, E.S.
Kuptsova, L.A. Shitova, N.V. Lebedeva) helped to demonstrate the participation
of glucose in the regulation of transcription of the chloroplast genome and in
regulation the photosynthesis at the genetic level36-38,41.
The
phenomenon of metabolic regulation of photosynthesis studied in model
experiments with non-metabolized glucose analogues was observed in
physiological experiments with hyper-accumulation of assimilates in the
chloroplast after filling the pool of storage polysaccharides. Transition of
photosynthetic cells to specialized biosynthesis is determined by a complex
chain of events that are genetically determined. This chain involves the
processes of synthesis and induced selective proteolysis of proteins. These
observations (G.L. Klyachko-Gurvich, T.S. Rudova) formed the basis for
controlled biosynthesis of algal biomass with determined amounts of
carbohydrates, lipids, or biologically active compounds 25,42-46,46-50.
In parallel
with the study of endogenous regulation of photosynthesis under excess
photosynthetic activity, Victor Semenenko developed the research in the area of
self-limitation of photosynthesis under CO2 defficiency51-62. Semenenko
maintained the hypothesis that low concentration of CO2 in our modern
atmosphere is one of global limiting factors forphotosynthesis of algae and of
C3 plants. In the early 70's, after the discovery of C4 photosynthesis, it was
accepted that the ability to concentrate CO2 in the cell is a distinctive
feature of C4 plants, whereas the C3 plants do not possess this ability. At
that time many researchers studied the pathways of carbon in C3 plants after
its interaction with RuBisCO, whereas the transport of CO2 into the cell was
considered as resistance to diffusion of CO2.
However, a
number of facts, such as a) discrepancy between the actual affinity of RuBisCo
to CO2 and the calculated its concentrations in the stroma; b) the increase in
photosynthetic affinity for CO2 during adaptation of cells to a decrease of
carbon dioxide in the environment; c) the ability of algae to grow in the
absence of CO2 in bicarbonate-containing media – all these facts contradicted
with the hypothesis of direct diffusion of CO2 to the centers of carboxylation
and showed that substrate supply for the dark reactions of photosynthesis is
under genetic control33,63,64.
Already in
his first article on this subject (1977) Victor Semenenko proposed and
experimentally confirmed the existence of the carbonic anhydrase system in
photosynthetic cells, which includes soluble and membrane-associated forms of
the enzyme62.
In 1981,
based on the detailed studies of the organization of carbonic anhydrase system
in different taxonomic groups of algae, its physiological and biochemical
properties, regulation of synthesis of different forms of carbonic anhydrase,
as well as adaptive reorganizations of their activities, Victor Semenenko and
his students and colleagues (N.A. Pronina, Z.M. Ramazanov) presented the
original model of the CO2-concentrating mechanism (CCM) in the algae59. This
has initiated the interest in this problem by many researchers.
One of the
major achievements was the discovery (Semenenko & Ramazanov) of the
regulatory role of the oxygenase function of RuBisCO in the induction of a
CO2-dependent form of carbonic anhydrase and in regulatory interactions between
photosynthesis, photorespiration and nuclear genetic apparatus of plant cells
in optimization of carbon nutrition in microalgae. It was shown that
glyoxylate, being a product of photorespiration, is the inducer of the
synthesis of carbonic anhydrase involved in the transport of Ci into the
chloroplast55,59,65,66.
The
theoretical works of Victor Semenenko may be supplemented by the hypothesis on
the importance of pyrenoid containing RuBisCO and carbonic anhydrase in the
concentration, generation, and fixation of CO2 in the chloroplast. Semenenko
& Vladimirova have been the first how showed localization of the RuBisCO in
the pyrenoid67-69. Later this line of work was developed further by N.A.
Pronina70-75.
The discovery in 1988 of carbonic anhydrase in
the thylakoid membranes, the kinetic studies of photochemical reactions in
chloroplasts in the presence of carbonic anhydrase inhibitors, and in CCM
mutants, showed the direct involvement of thylakoid carbonic anhydrase in the
control of the Calvin cycle. These data served as a serious argument in favor
of the shunting of CCM, which essence is in the transfer of HCO3 into the lumen
and in its carbonic-anhydrase-mediated transformation to CO2, which diffuses
into the stroma due to the gradient of concentrations51,52,54. The presented
model of the mechanism of concentration, generation and fixation of CO2 in the
chloroplasts of algae, which takes into account the pH of individual cellular
compartments, the selective properties of membranes, intracellular localization
of the carbonic anhydrases, RuBisCO, and photosystems, had analyzed in special
reviews and articles (S. Miyachi76, J.V.
Moroney77, J.A. Raven78, G. Samuelsson79). This model was recognized mostly by
all investigators of photosynthesis. The advantage of this model is also in the
fact that it induces a range of new directions in research of photosynthesis,
in particular, the integration of functions of carbonic anhydrase in
photosynthesis with the role of its isozymes in the process of respiration,
water photolysis and O2 evolution, that ensure the symmetry of the
photosynthetic and respiratory functions of the family of carbonic anhydrases
in the plant cell. The experimental data
and the conclusions allowed Victor Semenenko and co-workers to formulate the
concept of the functional role of CCM as a complete integrated system, in which
the crucial role is played by the compartmentalization, the selective
properties of membranes, the proton gradient, location and topology of the
carbonic anhydrase and the transmembrane transport of Ci. This concept significantly extends the concept of
photosynthetic metabolism.
Cited articles:
- Semenenko VE (1952) The
effect of starvation onthe light condition of the chloroplasts in leaves
of green plants. Proceedings of the
Fomin
Botanical Garden of
Kiev
State
University.
pp. 99-102. (Kiev State University,1952). in Russian.
- Semenenko
VE (1962) Mechanism of the processes of transition states in
photosynthesis. p. 1-
30.
in Russian.
- Semenenko
VE (1958) Apparatus for studying the kinetics of induction period of
photosynthesis, carbon dioxide gas analyzer with a differential for
thermistors. Sov. Plant Physiol. 5(6): 561-568.
- Semenenko
VE, Vladimirova MG (1961) Effect of space flight on board the satellite to
maintain viability of the culture of Chlorella. Sov. Plant Physiol.
8(6): 743-749.
- Semenenko
VE, Vladimirova MG (1962) Problems of space biology.
Sisakyan
NM (ed.), pp. 190-203 (
USSR
Academy
of Sciences,
Moscow).
in Russian.
- Semenenko
VE, Vladimirova MG (1962) Satellites. pp. 56-62 (
USSR
Academy of Sciences,
Moscow). in Russian.
- Ivanov
et al. (1967) The biological reactor. (Inventor's Certificate N 201 137,
15.06.1967). BI 17: 171-172,
1967. in Russian.
- Tsoglin
LN, Semenenko VE Polyakov AK (1967) The theoretical basis of the principle
of auto-competitive selection of productive forms of unicellular algae
based on mathematical modeling of the dynamics of population growth in
multicomponent flow culture. Biophysics 12 (4): 704-
714. in Russian.
- Tsoglin LN, Vladimirova MG, Semenenko VE (1970) Mathematical and experimental
simulation of autoselection of microalgae in a flow-through culture. Sov.
Plant Physiol. 17(6): 1129-1139.
- Semenenko
VE (1975) Photoregulation of plant metabolism and morphogenesis. pp.
135-157 (Nauka,
Moscow).
in Russian
- Semenenko
VE, Vladimirova MG, Orleanskaya OB (1967) The physiological
characteristics of Chlorella sp. K at high temperature extremes. I.
Uncoupling effect of extreme temperatures on cellular functions of
chlorella. Sov. Plant Physiol. 14(4): 612-625.
- Semenenko
VE Vladimirova MG, Orleanskaya OB, Raikov NI, Kovanova YS (1969) The
physiological characteristics of Chlorella sp. K at high
temperature extremes. II. Change biosynthesis, ultrastructure and activity
of the photosynthetic apparatus of Chlorella in dividing cell
function extreme temperatures. Sov. Plant Physiol. 16(2): 210-220.
- Bochacher
FM, Neimark VM, Semenenko VE,
Tsoglin
LN (1973) Apparatus for the cultivation of
algae. AC 377 030, 1973. Not to be published in open press. Inventor's
Certificate. Application N1617441 27.01.1971.
- Bochacher
FM, Borisenko ON, Otchenashenko IM, Semenenko VE, Tsoglin LN (1971)
Setting turbidistatic cultivation of microorganisms. Inventor's
Certificate N 326 874 10/22/1971.
- Tsoglin
LN, Avramova S, Gebov A, Dilov Ch, Semenenko VE (1980) Study of O2
gas exchange and optimization mode cultivation of algae in open settings
such as "Šetlík." Sov. Plant Physiol. 27(3): 644-652.
- Tsoglin LN, Yevstratov AV, Semenenko VE (1979) The use of microalgae for the
biosynthesis of C-compounds. Sov. Plant Physiol. 26 (1): 215-218.
- Vladimirova
MG, Semenenko VE (1977) The life of plants. pp. 367-376. (Education,
Moscow). in Russian.
- Semenenko
VE, Afanasyev VP (1972) to study the mechanisms of autoregulation of
photosynthesis. Reversible 2-deoxy-D-glucose repression effect of the photosynthetic
apparatus of the cell. Sov. Plant Physiol. 9(5): 1074-1081.
- Semenenko
VE (1978) Molecular biology of the endogenous regulation of
photosynthesis. Sov. Plant Physiol. 25(5): 903-921.
- Kuptsova
ES, Semenenko VE (1981) Light-dependent repressive action of glucose
analogs in the chloroplast. Sov. Plant Physiol. 28(4): 743-748.
- Semenenko
VE (1981) Metabolite regulation of chloroplast genome expression and the
activity of photosynthetic apparatus. Proceeding of the fifth
international congress on photosynthesis. G. Akoyunoglou (ed.) pp.
767-776. (BIS Services,
Philadelphia).
- Semenenko
VE (1982) Physiol. of photosynthesis. (Ed. Nichiporovich AA). pp. 164-187.
(Nauka,
Moscow).
in Russian.
- Tsoglin LN, Semenenko VE (1979) Increased productivity and efficiency of
photosynthesis by algae control population age structure. Proceedings of Xth
All-Union Conference, Kanev, 1979. pp. 294-303. (Naukova Dumka,
Kiev). in Russian.
- Tsoglin LN, Vladimirova MG, Semenenko VE (1976) Autoselection of microalgal
strains in a flowing culture. Proceedings of the XIth Research
Symposium, Scientific Coordination Meeting on I-184 of the CMEA. pp.
22-36. (Published by
Leningrad
State
University).
in Russian.
- Semenenko
VE, Vladimirova MG,
Tsoglin
LN, Tauts MI, Filippovskiy JN,
Klyachko-Gurvich GL, Kuznetsov ED, Kovanova ES, Raikov NI (1966)
Continuous cultivation of algae: controlled flow, physiological and
biochemical characteristics. I) Productivity and efficiency of utilization
of radiant energy during prolonged intensive cultivation of Chlorella.
In: "Controlled biosynthesis." pp. 75-86. (Nauka,
Moscow). in Russian.
- Tsoglin LN, Semenenko VE, Bochacher FM, Filippovskiy JN (1966) Device for the
controlled flow cultivation of algae with automatic measurement,
registration and regulation of the density of the suspension. In:
"Controlled biosynthesis." pp. 324-330. (Nauka,
Moscow). in Russian.
- Klimova
LA, Roshchin VV, Zvereva MG, Semenenko VE (1983) Reversible violations of
photosynthesis electron transport chain in intact Chlorella cells
under the action of the stereochemical analog of glucose. XI All-Union
Workshop on the cycle of substances in closed systems. pp. 50-56. (Naukova
Dumka,
Kiev).
in Russian.
- Zvereva
MG, Klimova LA, Semenenko VE (1980) Repression of rRNA synthesis and
activity of the breach of the chloroplast photochemical systems under the
action of 2-deoxy-D-glucose and hyper-accumulation of assimilates in Chlorella
cells. Sov. Plant Physiol. 27(6): 1218-
1228. in Russian.
- Semenenko
VE Kuptsova ES, Kasatkina T, Pronina NA, Vladimirova MG, Zvereva MG,
Kuznetsova LG (1979) Kinetic characteristics of the reversible repression
of protein synthesis and functional activity of the chloroplast
stereochemical analogues of glucose. pp. 313-320. In: “The Role of the
lower organisms in the circulation of substances in closed ecological
systems” (Proceedings of X All-Union Conference, Kanev, 1979, Naukova
Dumka, Kiev). in Russian.
- Zvereva
MG, Shubin LM, Klimova LA, Semenenko VE (1979) Reversible changes in the
spectra of low-temperature fluorescence of intact Chlorella cells
caused by repression of the photosynthetic apparatus by 2-deoxy-D-glucose.
Proc. Acad. Sci. USSR 244: 1244-
1247. in Russian.
- Semenenko
VE, Zvereva, MG (1972) Comparative study of restructuring in the direction
of the photobiosynthesis in two strains of Chlorella functions
under uncoupling action of extreme temperatures. Sov. Plant Physiol.
19(2): 229-
237. in
Russian.
- Semenenko
VE, Shitova LA,
LA
Shitova, Rudova TS, Pronina NA (1992) Regulatory
2-deoxy-D-glucose-resistant mutants of Chlorella vulgaris with
impaired metabolic system of negative regulation of expression of the
chloroplast genome of the end products of photosynthesis. Sov. Plant
Physiol. 39(6): 1135-1145.
- Semenenko
VE, Kasatkina TI, Rudova TS (1976) Reversible inhibition of protein
synthesis in fraction I under the influence 2-deoxy-D-glucose. Sov. Plant
Physiol. 23(6): 1225-1231.
- Kuptsova
ES, Semenenko VE (1986) The dependence of the repressive action of glucose
analogs in the chloroplast of the spectral composition of light. Sov.
Plant Physiol. 33(4): 699-708.
- Kuptsova
ES, Semenenko VE (1983) The relationship between the structure of glucose
analogues and their repressive action in the chloroplast. Sov. Plant
Physiol. 30(5): 1006-1014.
- Semenenko
VE (1988) Photosynthesis and production process. pp. 69-81 (Nauka,
Moscow). in Russian.
- Semenenko
V.E. (1996) Physiological and genetic potentials of microalgae and
molecular biology aspects of photoautotrophic biosyntheses biotechnology.
TIT Symposium Microalgal Biotechnology: Basics and Applications. pp. 1-8.
(
Osaka,
Japan).
- Shitova
LA,
Meshcheryakov
AB, Semenenko VE (1994) Regulatory
mutants of Chlorella c impaired transport system of exogenous glucose into
the cell. Sov. Plant Physiol. 41 (2): 223-226.
- Semenenko
VE, Shitova LA (1991) A method for the selection of regulatory mutants of
photosynthetic algae and algae strain Chlorella sp. K – the
producer of carbohydrates. Inventor's certificate N1654337. 02/08/1991.
- Lebedeva
NV, Semenenko VE (2000) Regulation of photosynthesis by glucose and
its stereochemical analogue in the cyanobacterium Synechocystis sp.
PCC 6803. Russ. J. Plant Physiol. 47(5): 662-667.
- Lebedeva
NV, Semenenko VE (1992) The 2-deoxy-D-glucose effect on the mRNA levels ofpsbA, psbD and desA genes in Synechocystis PCC6803.
Research in Photosynthesis. Murata N. (ed.), pp. 457-460 (Kluwer Academic
Publishers,
Dordrecht, The
Netherlands).
- Yurieva
MI, Klyachko-Gurvich GL, Semenenko VE, Temnykh AA (1990) A method of
biomass production of the unicellular alga Porphyridium enriched
with eicosapentaenoic and arachidonic acid. Inventor's certificate
N1609827, 1.08.1990.
- Ramazanov
ZM, Klyachko-Gurvich GL, Ksenofontov AL, Semenenko VE (1988) Effect of
suboptimal temperature on the content of b-carotene and lipids in
halophilic alga Dunaliella salina. Sov. Plant Physiol. 35(5):
864-872.
- Klyachko-Gurvich
GL, Tauts MI, Semenenko VE (1985) Microorganisms in artificial ecosystems.
pp. 53-61. (Nauka,
Novosibirsk).
in Russian.
- Klyachko-Gurvich
GL, Semenov AN, Semenenko VE (1980) Lipid metabolism in the chloroplasts
of Chlorella cells to adapt to lower light conditions. Sov. Plant
Physiol. 27(2): 370-379.
- Klyachko-Gurvich
GL, Rudova TS, Kovanova ES, Semenenko VE (1973) Effect of imidazole on the
exchange of fatty acids in the restoration of Chlorella cells after
nitrogen starvation. Sov. Plant Physiol. 20(3): 326-331.
- Klyachko-Gurvich
GL, Semenenko VE (1966) Biology of autotrophic organisms. pp. 154-159.
(Moscow State University, Moscow, 1966). In Russian.
- Klyachko-Gurvich
GL, Semenenko VE (1965) Some physiological and biochemical aspects aimed
to provide valuable metabolites and substances under conditions of
intensive culture of algae. (The study of intensive algal culture). pp.
143-151.
Prague.
Proceedings of the IIId coordination meeting of the CMEA. In
Russian.
- Semenenko
VE, Ramazanov ZM, Rudova TS, Abdullaev AA (1987) A method for cultivation
of microalgae Dunaliella salina. Inventor's certificate N1513911.
08.06.1989. In Russian.
- Semenenko
VE, Rudova TS (1975) Effect of cycloheximide on the biosynthesis process
of restructuring the cells of Chlorella caused by nitrogen
starvation. Sov. Plant Physiol. 22(5): 958-965.
- Furnadzhieva
S, Pronina NA, Andreeva R, Petkov G, Semenenko VE (2001) Involvement of
carbonic anhydrase in the bicarbonate ion assimilation by cells of Chlorella
and Scenedesmus. Russ. J. Plant Physiol. 37(1): 22-30.
- Pronina
NA,
Zhila
NM, Semenenko VE (1999) Two forms of
carbonic anhydrase in the cells of Dunaliella salina; isolation and
properties. Sov. Plant Physiol. 46(1): 62-68.
- Pronina
NA, Semenenko VE (1991) Molecular and cellular organization of CO2
concentrating mechanisms in photoautotrophic cells of algae. Algologia
1(2): 80-92.
- Pronina
NA, Semenenko VE (1988) Localization of carbonic anhydrase bound to
membranes of cells of Chlorella. Sov. Plant Physiol. 35(1): 51-61.
- Ramazanov
ZM, N. Pronina NA, Semenenko VE (1984) On the oxygen dependence of the
induction of synthesis of CO2-dependent soluble form of
carbonic anhydrase in Chlorella cells. Sov. Plant Physiol. 31(3):
448-455.
- Kasatkina
TI, Pronina NA, Semenenko VE (1984) Quantitative isolation, fractionation
and characterization of ribulose-1,5-bisphosphatcarboxylase from Chlorella
cells. Sov. Plant Physiol. 31(1): 130-140.
- Abramova
S, Pronina NA, Semenenko V, Georgiev D, Peshev IS (1984) Carbonic
anhysdase activity and assimilation of bicarbonate ion cells Chlorella
and Scenedesmus. Hydrobiologija 20: 8-15.
- Pronina
NA, Semenenko VE (1984) Localization of membrane-bound and soluble forms
of carbonic anhydrase in Chlorella cells. Sov. Plant Physiol.
31(2): 241-251.
- Pronina
NA, Ramazanov ZM, Semenenko VE (1981) The dependence of the activity of
the carbonic anhydrase activity of Chlorella cells on the concentration of
CO2. Sov. Plant Physiol. 28(3): 494-502.
- Pronina
NA, Abramova S, Georgiev D, Semenenko VE (1981) Dynamics of carbonic
anhydrase activity of Chlorella and Scenedesmus during
adaptation of cells to high light intensity and low concentrations of CO2.
Sov. Plant Physiol. 28(1): 43-52.
- Semenenko
VE, Abramova S, Georgiev D, Pronina NA (1979) On the light dependence of
carbonic anhydrase activity of Chlorella and Scenedesmus
cells. Sov. Plant Physiol. 26(5): 1069-1075.
- Semenenko
VE, Abramova S, Georgiev D, Pronina NA (1977) Comparative study of
carbonic anhydrase activity and localization in cells of Chlorella
and Scenedesmus. Sov. Plant Physiol. 24(5): 1055-1059.
- Kasatkina
TI, Vedeneyev AN, Semenenko VE (1985) Regulation of the synthesis of
ribulose-1,5-bisphosphate carboxylase and its subunits in the cells. In:
"Microorganisms in artificial ecosystems." p. 97-102. (Nauka,
Novosibirsk). In
Russian.
- Kasatkina
TI, Tikhonov NG, Vladimirova MG, Volodarsky AD, Semenenko VE (1974) Study
of the antigenic structure of two strains of Chlorella, with a
variety of physiological and biochemical properties. Sov. Plant Physiol.
21(4): 752-755.
- Ramazanov
ZM, Semenenko VE (1988) The dependence of the CO2-dependent
form of carbonic anhydrase on the light intensity and photosynthesis. Sov.
Plant Physiol. 35(3): 438-443.
- Ramazanov
ZM, Semenenko VE (1986) The participation of products of photorespiration
in CO2-dependent induction of a form of carbonic anhydrase.
Sov. Plant Physiol. 33(5): 864-872.
- Markelova
AG, Vladimirova MG, Semenenko VE (1990) Ultrastructural localization of
RuBisCO in algae cells. Sov. Plant Physiol. 37(5): 907-911.
- Markelova
AG, Shapiguzov YM, Vladimirova MG, Semenenko VE (1985) Quantitative
estimation of immunofluorescence of pyrenoid as a giant
carboxysome-containing compartment. In: "Microorganisms in artificial
ecosystems." pp. 35-41. (Nauka,
Novosibirsk).
In Russian.
- Vladimirova
MG, Markelova AG, Semenenko VE (1982) Identification of the localization
of RuBisCO in the pyrenoid of a unicellular algae by immunocytochemical
method. Sov. Plant Physiol. 29(5): 941-950.
- Dudoladova
MV, Kupriyanova EV, Markelova AG, Sinetova MP, Allakhverdiev SI, Pronina
NA (2007) The thylakoid carbonic anhydrase associated with photosystem II
is the component of inorganic carbon accumulating system in cells of
halo-and alkaliphilic cyanobacterium Rhabdoderma lineare. Biochim.
Biophys. Acta 1767: 616-623.
- Kupriyanova
E, Villarejo A, Markelova A, Gerasimenko L, Zavarzin G, Samuelsson G, Los
DA, Pronina NA (2007) Extracellular carbonic anhydrases of the
stromatolite-forming cyanobacterium Microcoleus chthonoplastes.
Microbiology SGM 153: 1149-1156.
- Markelova
AG, Sinetova MA, Kupriyanova EV, Pronina NA (2009) Distribution and
functional role of carbonic anhydrase Cah3 associated with thylakoid
membranes in the chloroplast and pyrenoid of Chlamydomonas reinhardtii.
Russ. J. Plant Physiol. 56 (6): 761-798.
- Kupriyanova
EV, Pronina NA (2011) Carbonic anhydrase: Enzyme that has transformed the
biosphere. Russ. J. Plant Physiol. 58 (2): 197-209.
- Kupriyanova
EV, Sinetova MA, Markelova AG, Allakhverdiev SI, Los DA, Pronina NA (2011)
Extracellular ?-class carbonic anhydrase of the alkaliphilic
cyanobacterium Microcoleus chthonoplastes. J. Photochem. Photobiol.
B: Biol. 103: 78-86.
- Sinetova
MA, Kupriyanova EV, Markelova AG, Allakhverdiev SI, Pronina NA (2012)
Identification and functional role of the carbonic anhydrase Cah3 in
thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii.
Biochim. Biophys. Acta 1817: 1248–1255.
- Miyachi
S, Iwasaki I, Shiraiwa Y (2003) Historical perspective on microalgal and
cyanobacterial acclimation to low-and extremely high-CO2
conditions. Photosynthesis Research 77: 139-153.
- Borkhsenious
ON, Mason CB, Moroney JV (1998) The intracellular localization of
ribulose-1,5-bisphosphate carboxylase/oxygenase in Chlamydomonas
reinhardtii. Plant Physiol. 116: 1585-1591.
- Raven
JA, Beardall J (2004) Carbon acquisition mechanisms of algae: Carbon
dioxide diffusion and carbon dioxide concentrating mechanisms. In:
Photosynthesis in Algae. Advances in Photosynthesis and Respiration.
14(3): 225-244.
- Karlsson J, Clarke AK, Chen
ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G (1998) A novel
a-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas
reinhardtii is required for growth at ambient CO2. EMBO J.
17(5): 1208-1216.
|
|