TY - JOUR

T1 - Absence of Complex I Implicates Rearrangement of the Respiratory Chain in European Mistletoe

AU - Senkler, Jennifer

AU - Rugen, Nils

AU - Eubel, Holger

AU - Hegermann, Jan

AU - Braun, Hans Peter

N1 - Funding information: We thank Michael Senkler for support with data evaluation and for developing and maintaining the GelMap and ComplexomeMap portals. We thank Claudia Probst for support in photo documentation of V. album in natural environment. This work was supported by Leibniz Universität Hannover and by the Deutsche Forschungsgemeinschaft (grant no. EU54/4-1 to H.E.).

PY - 2018/5/21

Y1 - 2018/5/21

N2 - The mitochondrial oxidative phosphorylation (OXPHOS) system, which is based on the presence of five protein complexes, is in the very center of cellular ATP production. Complexes I to IV are components of the respiratory electron transport chain that drives proton translocation across the inner mitochondrial membrane. The resulting proton gradient is used by complex V (the ATP synthase complex) for the phosphorylation of ADP. Occurrence of complexes I to V is highly conserved in eukaryotes, with exceptions being restricted to unicellular parasites that take up energy-rich compounds from their hosts. Here we present biochemical evidence that the European mistletoe (Viscum album), an obligate semi-parasite living on branches of trees, has a highly unusual OXPHOS system. V. album mitochondria completely lack complex I and have greatly reduced amounts of complexes II and V. At the same time, the complexes III and IV form remarkably stable respiratory supercomplexes. Furthermore, complexome profiling revealed the presence of 150 kDa complexes that include type II NAD(P)H dehydrogenases and an alternative oxidase. Although the absence of complex I genes in mitochondrial genomes of mistletoe species has recently been reported, this is the first biochemical proof that these genes have not been transferred to the nuclear genome and that this respiratory complex indeed is not assembled. As a consequence, the whole respiratory chain is remodeled. Our results demonstrate that, in the context of parasitism, multicellular life can cope with lack of one of the OXPHOS complexes and give new insights into the life strategy of mistletoe species.

AB - The mitochondrial oxidative phosphorylation (OXPHOS) system, which is based on the presence of five protein complexes, is in the very center of cellular ATP production. Complexes I to IV are components of the respiratory electron transport chain that drives proton translocation across the inner mitochondrial membrane. The resulting proton gradient is used by complex V (the ATP synthase complex) for the phosphorylation of ADP. Occurrence of complexes I to V is highly conserved in eukaryotes, with exceptions being restricted to unicellular parasites that take up energy-rich compounds from their hosts. Here we present biochemical evidence that the European mistletoe (Viscum album), an obligate semi-parasite living on branches of trees, has a highly unusual OXPHOS system. V. album mitochondria completely lack complex I and have greatly reduced amounts of complexes II and V. At the same time, the complexes III and IV form remarkably stable respiratory supercomplexes. Furthermore, complexome profiling revealed the presence of 150 kDa complexes that include type II NAD(P)H dehydrogenases and an alternative oxidase. Although the absence of complex I genes in mitochondrial genomes of mistletoe species has recently been reported, this is the first biochemical proof that these genes have not been transferred to the nuclear genome and that this respiratory complex indeed is not assembled. As a consequence, the whole respiratory chain is remodeled. Our results demonstrate that, in the context of parasitism, multicellular life can cope with lack of one of the OXPHOS complexes and give new insights into the life strategy of mistletoe species.

KW - complex I

KW - complexome profiling

KW - mistletoe

KW - mitochondria

KW - NADH ubiquinone oxidoreductase complex

KW - OXPHOS system

KW - respiratory chain

KW - Viscum album

KW - Electron Transport/physiology

KW - Mitochondria/metabolism

KW - Oxidative Phosphorylation

KW - Viscum album/genetics

KW - Electron Transport Complex I/genetics

UR - http://www.scopus.com/inward/record.url?scp=85046172153&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2018.03.050

DO - 10.1016/j.cub.2018.03.050

M3 - Article

C2 - 29731306

AN - SCOPUS:85046172153

VL - 28

SP - 1606-1613.e4

JO - Current biology

JF - Current biology

SN - 0960-9822

IS - 10

ER -