Inheritance of the reduced mitochondria of Giardia intestinalis
is coupled to the flagellar maturation cycle

J 2021

Inheritance of the reduced mitochondria of Giardia intestinalis is coupled to the flagellar maturation cycle

TUMOVA, P., L. VOLEMAN, A. KLINGL, E. NOHYNKOVA, G. WANNER et. al.

Základní údaje

Originální název

Inheritance of the reduced mitochondria of Giardia intestinalis is coupled to the flagellar maturation cycle

Autoři

TUMOVA, P., L. VOLEMAN, A. KLINGL, E. NOHYNKOVA, G. WANNER a P. DOLEZAL

Vydání

BMC BIOLOGY, 2021, 1741-7007

Další údaje

Jazyk

angličtina

Typ výsledku

Článek v odborném periodiku

Obor

10600 1.6 Biological sciences

Stát vydavatele

Velká Británie a Severní Irsko

Utajení

není předmětem státního či obchodního tajemství

Odkazy

URL

Impakt faktor

Impact factor: 7.364

Kód RIV

RIV/00216224:14740/21:00124513

Organizační jednotka

Středoevropský technologický institut

DOI

http://dx.doi.org/10.1186/s12915-021-01129-7

UT WoS

000695452800005

Klíčová slova anglicky

Mitochondrial inheritanceMitosomesmitochondrial evolutionFlagellumCytoskeletonCell cycleMitochondrial divisionProtistGiardia

Štítky

ne MU, rivok

Příznaky

Mezinárodní význam, Recenzováno

Změněno: 18. 5. 2022 15:04, Mgr. Pavla Foltynová, Ph.D.

Anotace

V originále

Background The presence of mitochondria is a distinguishing feature between prokaryotic and eukaryotic cells. It is currently accepted that the evolutionary origin of mitochondria coincided with the formation of eukaryotes and from that point control of mitochondrial inheritance was required. Yet, the way the mitochondrial presence has been maintained throughout the eukaryotic cell cycle remains a matter of study. Eukaryotes control mitochondrial inheritance mainly due to the presence of the genetic component; still only little is known about the segregation of mitochondria to daughter cells during cell division. Additionally, anaerobic eukaryotic microbes evolved a variety of genomeless mitochondria-related organelles (MROs), which could be theoretically assembled de novo, providing a distinct mechanistic basis for maintenance of stable mitochondrial numbers. Here, we approach this problem by studying the structure and inheritance of the protist Giardia intestinalis MROs known as mitosomes. Results We combined 2D stimulated emission depletion (STED) microscopy and focused ion beam scanning electron microscopy (FIB/SEM) to show that mitosomes exhibit internal segmentation and conserved asymmetric structure. From a total of about forty mitosomes, a small, privileged population is harnessed to the flagellar apparatus, and their life cycle is coordinated with the maturation cycle of G. intestinalis flagella. The orchestration of mitosomal inheritance with the flagellar maturation cycle is mediated by a microtubular connecting fiber, which physically links the privileged mitosomes to both axonemes of the oldest flagella pair and guarantees faithful segregation of the mitosomes into the daughter cells. Conclusion Inheritance of privileged Giardia mitosomes is coupled to the flagellar maturation cycle. We propose that the flagellar system controls segregation of mitochondrial organelles also in other members of this supergroup (Metamonada) of eukaryotes and perhaps reflects the original strategy of early eukaryotic cells to maintain this key organelle before mitochondrial fusion-fission dynamics cycle as observed in Metazoa was established.

Návaznosti

90127, velká výzkumná infrastruktura

Název: CIISB II

Citovat

TUMOVA, P., L. VOLEMAN, A. KLINGL, E. NOHYNKOVA, G. WANNER a P. DOLEZAL. Inheritance of the reduced mitochondria of Giardia intestinalis is coupled to the flagellar maturation cycle. BMC BIOLOGY. 2021, roč. 19, č. 1, s. 193-212. ISSN 1741-7007. Dostupné z: https://dx.doi.org/10.1186/s12915-021-01129-7.

@article{1846470,
   author = {Tumova, P. and Voleman, L. and Klingl, A. and Nohynkova, E. and Wanner, G. and Dolezal, P.},
   article_number = {1},
   doi = {http://dx.doi.org/10.1186/s12915-021-01129-7},
   keywords = {Mitochondrial inheritanceMitosomesmitochondrial evolutionFlagellumCytoskeletonCell cycleMitochondrial divisionProtistGiardia},
   language = {eng},
   issn = {1741-7007},
   journal = {BMC BIOLOGY},
   title = {Inheritance of the reduced mitochondria of Giardia intestinalis is coupled to the flagellar maturation cycle},
   url = {https://bmcbiol.biomedcentral.com/track/pdf/10.1186/s12915-021-01129-7.pdf},
   volume = {19},
   year = {2021}
}

TY  - JOUR
ID  - 1846470
AU  - Tumova, P. - Voleman, L. - Klingl, A. - Nohynkova, E. - Wanner, G. - Dolezal, P.
PY  - 2021
TI  - Inheritance of the reduced mitochondria of Giardia intestinalis is coupled to the flagellar maturation cycle
JF  - BMC BIOLOGY
VL  - 19
IS  - 1
SP  - 193
EP  - 193
SN  - 17417007
KW  - Mitochondrial inheritanceMitosomesmitochondrial evolutionFlagellumCytoskeletonCell cycleMitochondrial divisionProtistGiardia
UR  - https://bmcbiol.biomedcentral.com/track/pdf/10.1186/s12915-021-01129-7.pdf
N2  - Background The presence of mitochondria is a distinguishing feature between prokaryotic and eukaryotic cells. It is currently accepted that the evolutionary origin of mitochondria coincided with the formation of eukaryotes and from that point control of mitochondrial inheritance was required. Yet, the way the mitochondrial presence has been maintained throughout the eukaryotic cell cycle remains a matter of study. Eukaryotes control mitochondrial inheritance mainly due to the presence of the genetic component; still only little is known about the segregation of mitochondria to daughter cells during cell division. Additionally, anaerobic eukaryotic microbes evolved a variety of genomeless mitochondria-related organelles (MROs), which could be theoretically assembled de novo, providing a distinct mechanistic basis for maintenance of stable mitochondrial numbers. Here, we approach this problem by studying the structure and inheritance of the protist Giardia intestinalis MROs known as mitosomes. Results We combined 2D stimulated emission depletion (STED) microscopy and focused ion beam scanning electron microscopy (FIB/SEM) to show that mitosomes exhibit internal segmentation and conserved asymmetric structure. From a total of about forty mitosomes, a small, privileged population is harnessed to the flagellar apparatus, and their life cycle is coordinated with the maturation cycle of G. intestinalis flagella. The orchestration of mitosomal inheritance with the flagellar maturation cycle is mediated by a microtubular connecting fiber, which physically links the privileged mitosomes to both axonemes of the oldest flagella pair and guarantees faithful segregation of the mitosomes into the daughter cells. Conclusion Inheritance of privileged Giardia mitosomes is coupled to the flagellar maturation cycle. We propose that the flagellar system controls segregation of mitochondrial organelles also in other members of this supergroup (Metamonada) of eukaryotes and perhaps reflects the original strategy of early eukaryotic cells to maintain this key organelle before mitochondrial fusion-fission dynamics cycle as observed in Metazoa was established.
ER  -

TUMOVA, P., L. VOLEMAN, A. KLINGL, E. NOHYNKOVA, G. WANNER a P. DOLEZAL. Inheritance of the reduced mitochondria of Giardia intestinalis is coupled to the flagellar maturation cycle. \textit{BMC BIOLOGY}. 2021, roč.~19, č.~1, s.~193-212. ISSN~1741-7007. Dostupné z: https://dx.doi.org/10.1186/s12915-021-01129-7.

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