TY - JOUR
T1 - Metabolic Capacity of Mitochondrion-related Organelles in the Free-living Anaerobic Stramenopile Cantina marsupialis
AU - Noguchi, Fumiya
AU - Shimamura, Shigeru
AU - Nakayama, Takuro
AU - Yazaki, Euki
AU - Yabuki, Akinori
AU - Hashimoto, Tetsuo
AU - Inagaki, Yuji
AU - Fujikura, Katsunori
AU - Takishita, Kiyotaka
N1 - Funding Information:
We are grateful to Drs. Jan Andersson (Uppsala University) and Courtney Stairs (Dalhousie University) for providing alignments for phylogenetic analyses. We also thank Drs. Goro Tanifuji (University of Tsukuba) and Miyuki Nishijima (JAMSTEC) for useful comments about the handling of RNA-seq data and HPLC data, respectively. This work was supported by grants from the Japanese Society for the Promotion of Science awarded to K.T. (No. 24117527), Y.I. (No. 23117006), and T.H. (No. 23117005).
Publisher Copyright:
© 2015 Elsevier GmbH.
PY - 2015/11/1
Y1 - 2015/11/1
N2 - Functionally and morphologically degenerate mitochondria, so-called mitochondrion-related organelles (MROs), are frequently found in eukaryotes inhabiting hypoxic or anoxic environments. In the last decade, MROs have been discovered from a phylogenetically broad range of eukaryotic lineages and these organelles have been revealed to possess diverse metabolic capacities. In this study, the biochemical characteristics of an MRO in the free-living anaerobic protist Cantina marsupialis, which represents an independent lineage in stramenopiles, were inferred based on RNA-seq data. We found transcripts for proteins known to function in one form of MROs, the hydrogenosome, such as pyruvate:ferredoxin oxidoreductase, iron-hydrogenase, acetate:succinate CoA-transferase, and succinyl-CoA synthase, along with transcripts for acetyl-CoA synthetase (ADP-forming). These proteins possess putative mitochondrial targeting signals at their N-termini, suggesting dual ATP generation systems through anaerobic pyruvate metabolism in Cantina MROs. In addition, MROs in Cantina were also shown to share several features with canonical mitochondria, including amino acid metabolism and an "incomplete" tricarboxylic acid cycle. Transcripts for all four subunits of complex II (CII) of the electron transport chain were detected, while there was no evidence for the presence of complexes I, III, IV, or F1Fo ATPase. Cantina MRO biochemistry challenges the categories of mitochondrial organelles recently proposed.
AB - Functionally and morphologically degenerate mitochondria, so-called mitochondrion-related organelles (MROs), are frequently found in eukaryotes inhabiting hypoxic or anoxic environments. In the last decade, MROs have been discovered from a phylogenetically broad range of eukaryotic lineages and these organelles have been revealed to possess diverse metabolic capacities. In this study, the biochemical characteristics of an MRO in the free-living anaerobic protist Cantina marsupialis, which represents an independent lineage in stramenopiles, were inferred based on RNA-seq data. We found transcripts for proteins known to function in one form of MROs, the hydrogenosome, such as pyruvate:ferredoxin oxidoreductase, iron-hydrogenase, acetate:succinate CoA-transferase, and succinyl-CoA synthase, along with transcripts for acetyl-CoA synthetase (ADP-forming). These proteins possess putative mitochondrial targeting signals at their N-termini, suggesting dual ATP generation systems through anaerobic pyruvate metabolism in Cantina MROs. In addition, MROs in Cantina were also shown to share several features with canonical mitochondria, including amino acid metabolism and an "incomplete" tricarboxylic acid cycle. Transcripts for all four subunits of complex II (CII) of the electron transport chain were detected, while there was no evidence for the presence of complexes I, III, IV, or F1Fo ATPase. Cantina MRO biochemistry challenges the categories of mitochondrial organelles recently proposed.
KW - Anoxic
KW - Hydrogenosomes
KW - Mitochondria
KW - Stramenopiles
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U2 - 10.1016/j.protis.2015.08.002
DO - 10.1016/j.protis.2015.08.002
M3 - Article
C2 - 26436880
AN - SCOPUS:84943420764
VL - 166
SP - 534
EP - 550
JO - Archiv fur Protistenkunde
JF - Archiv fur Protistenkunde
SN - 1434-4610
IS - 5
ER -