Role of pyrenoids in the CO2-concentrating mechanism

Comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas (Volvocales)

Eiko Morita, Toshihiko Abe, Mikio Tsuzuki, Shoko Fujiwara, Norihiro Sato, Aiko Hirata, Kintake Sonoike, Hisayoshi Nozaki

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

The morphology of the pyrenoid and the physiology of the CO2-concentrating mechanism (CCM) were investigated in Chlamydomonas (Cd.) mutabilis Gerloff UTEX 578, Cal. radiata Deason et Bold UTEX 966, Cd. augustae Skuja UTEX 1969, Cd. macrostellata Lund SAG 72.81, Cd. bipapillata Bourrelly SAG 11-47, and Chloromonas (Cr.) insignis Gerloff et Ettl NIES-447, all of which are closely related phylogenetically to the pyrenoid-less strains of Chloromonas. In the chloroplasts of Cd. mutabilis UTEX 578, Cd. radiata UTEX 966, Cd. augustae UTEX 1969, and Cd. macrostellata SAG 72.81, a typical, spheroidal, electron-dense pyrenoid matrix surrounded by starch granules was present, and ribulose-1.5-bisphosphate carboxylase/oxygenase (Rubisco; EC 4.1.1.39) molecules were highly concentrated in the pyrenoid matrix. On the other hand, while the pyrenoid matrix of Cr. insignis NIES-447 was electrondense that of Cd. hipapillata SAG 11-47 was not, and neither was surrounded by starch granules. The pyrenoid matrices of these two species exhibited a higher concentration of Rubisco molecules than the thylakoid region (thylakoid and stroma) of the chloroplasts; however, the densities of Rubisco molecules in these pyrenoid matrices were low compared with those of the other four Chlamydomonas strains examined in this study and that of Cd. reinhardtii Dangeard. In all six strains examined, the presence of the CCM was indicated by relatively high photosynthetic affinities for CO2 (low values of K0.5(CO2)). However, differences in the inorganic carbon (Ci) pools were recognized in relation to the differences in pyrenoid morphology among the strains. In the typical pyrenoid-containing strains. Cd. mutabilis UTEX 578 and Cd. radiata UTEX 966, the ratio of internal to external inorganic carbon was about 20, while in Cr. insignis NIES-447 and Cd. hipapillata SAG 11-47 the ratio was only 2-3 similar to the two pyrenoid-less, CCM-containing strains of Chloromonas previously examined (E. Morita et al., 1998, Planta 204: 269-276). It is thus speculated that the presence of typical pyrenoids with a high concentration of Rubisco molecules is related to the formation of large Ci pools in the CCM. Detailed phylogenetic relationships among these Chlamydomonas/Chloromonas strains and the pyrenoid-less Chloromonas strains previously investigated were inferred based on the sequence of rbcL, the gene for the large subunit of Rubisco. Two monophyletic groups were resolved with high bootstrap values. Based on the tree topology resolved, it was inferred that loss of the typical pyrenoids accompanied by a decrease in intracellular Ci pools might have taken place independently in the two groups.

Original languageEnglish
Pages (from-to)365-372
Number of pages8
JournalPlanta
Volume208
Issue number3
DOIs
Publication statusPublished - 1999
Externally publishedYes

Fingerprint

Comparative Physiology
Chlamydomonas
concentrating
physiology
Ribulose-Bisphosphate Carboxylase
phylogeny
ribulose-bisphosphate carboxylase
Thylakoids
Chloroplasts
Chlamydomonadales
starch granules
thylakoids
Starch
Carbon
chloroplasts
Chlamydomonas reinhardtii
Oxygenases

Keywords

  • Chlamydomonas
  • Chloromonas
  • CO/ concentrating mechanism
  • Molecular phylogeny
  • Pyrenoid
  • Ribulose-1,5-bisphosphate carboxylase/oxygenase

ASJC Scopus subject areas

  • Plant Science

Cite this

Role of pyrenoids in the CO2-concentrating mechanism : Comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas (Volvocales). / Morita, Eiko; Abe, Toshihiko; Tsuzuki, Mikio; Fujiwara, Shoko; Sato, Norihiro; Hirata, Aiko; Sonoike, Kintake; Nozaki, Hisayoshi.

In: Planta, Vol. 208, No. 3, 1999, p. 365-372.

Research output: Contribution to journalArticle

Morita, Eiko ; Abe, Toshihiko ; Tsuzuki, Mikio ; Fujiwara, Shoko ; Sato, Norihiro ; Hirata, Aiko ; Sonoike, Kintake ; Nozaki, Hisayoshi. / Role of pyrenoids in the CO2-concentrating mechanism : Comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas (Volvocales). In: Planta. 1999 ; Vol. 208, No. 3. pp. 365-372.
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TY - JOUR

T1 - Role of pyrenoids in the CO2-concentrating mechanism

T2 - Comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas (Volvocales)

AU - Morita, Eiko

AU - Abe, Toshihiko

AU - Tsuzuki, Mikio

AU - Fujiwara, Shoko

AU - Sato, Norihiro

AU - Hirata, Aiko

AU - Sonoike, Kintake

AU - Nozaki, Hisayoshi

PY - 1999

Y1 - 1999

N2 - The morphology of the pyrenoid and the physiology of the CO2-concentrating mechanism (CCM) were investigated in Chlamydomonas (Cd.) mutabilis Gerloff UTEX 578, Cal. radiata Deason et Bold UTEX 966, Cd. augustae Skuja UTEX 1969, Cd. macrostellata Lund SAG 72.81, Cd. bipapillata Bourrelly SAG 11-47, and Chloromonas (Cr.) insignis Gerloff et Ettl NIES-447, all of which are closely related phylogenetically to the pyrenoid-less strains of Chloromonas. In the chloroplasts of Cd. mutabilis UTEX 578, Cd. radiata UTEX 966, Cd. augustae UTEX 1969, and Cd. macrostellata SAG 72.81, a typical, spheroidal, electron-dense pyrenoid matrix surrounded by starch granules was present, and ribulose-1.5-bisphosphate carboxylase/oxygenase (Rubisco; EC 4.1.1.39) molecules were highly concentrated in the pyrenoid matrix. On the other hand, while the pyrenoid matrix of Cr. insignis NIES-447 was electrondense that of Cd. hipapillata SAG 11-47 was not, and neither was surrounded by starch granules. The pyrenoid matrices of these two species exhibited a higher concentration of Rubisco molecules than the thylakoid region (thylakoid and stroma) of the chloroplasts; however, the densities of Rubisco molecules in these pyrenoid matrices were low compared with those of the other four Chlamydomonas strains examined in this study and that of Cd. reinhardtii Dangeard. In all six strains examined, the presence of the CCM was indicated by relatively high photosynthetic affinities for CO2 (low values of K0.5(CO2)). However, differences in the inorganic carbon (Ci) pools were recognized in relation to the differences in pyrenoid morphology among the strains. In the typical pyrenoid-containing strains. Cd. mutabilis UTEX 578 and Cd. radiata UTEX 966, the ratio of internal to external inorganic carbon was about 20, while in Cr. insignis NIES-447 and Cd. hipapillata SAG 11-47 the ratio was only 2-3 similar to the two pyrenoid-less, CCM-containing strains of Chloromonas previously examined (E. Morita et al., 1998, Planta 204: 269-276). It is thus speculated that the presence of typical pyrenoids with a high concentration of Rubisco molecules is related to the formation of large Ci pools in the CCM. Detailed phylogenetic relationships among these Chlamydomonas/Chloromonas strains and the pyrenoid-less Chloromonas strains previously investigated were inferred based on the sequence of rbcL, the gene for the large subunit of Rubisco. Two monophyletic groups were resolved with high bootstrap values. Based on the tree topology resolved, it was inferred that loss of the typical pyrenoids accompanied by a decrease in intracellular Ci pools might have taken place independently in the two groups.

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KW - Chloromonas

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KW - Pyrenoid

KW - Ribulose-1,5-bisphosphate carboxylase/oxygenase

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