Genome Analysis of Structure–Function Relationships in Respiratory Complex I, an Ancient Bioenergetic Enzyme

Esposti, Mauro Degli

doi:10.1093/gbe/evv239

Cited by 17 publications

(41 citation statements)

References 118 publications

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“…We also confirmed the previously noted variability of bivalve residue 43 of the same gene (Degli Esposti 2015; fig. 3), which is also part of the Q reacting chamber (Baradaran et al.…”

Section: Discussionsupporting

confidence: 92%

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Burrowers from the Past: Mitochondrial Signatures of Ordovician Bivalve Infaunalization

Plazzi

Puccio

Passamonti

2017

Genome Biology and Evolution

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Bivalves and gastropods are the two largest classes of extant molluscs. Despite sharing a huge number of features, they do not share a key ecological one: gastropods are essentially epibenthic, although most bivalves are infaunal. However, this is not the ancestral bivalve condition; Cambrian forms were surface crawlers and only during the Ordovician a fundamental infaunalization process took place, leading to bivalves as we currently know them. This major ecological shift is linked to the exposure to a different redox environoments (hypoxic or anoxic) and with the Lower Devonian oxygenation event. We investigated selective signatures on bivalve and gastropod mitochondrial genomes with respect to a time calibrated mitochondrial phylogeny by means of dN/dS ratios. We were able to detect 1) a major signal of directional selection between the Ordovician and the Lower Devonian for bivalve mitochondrial Complex I, and 2) an overall higher directional selective pressure on bivalve Complex V with respect to gastropods. These and other minor dN/dS patterns and timings are discussed, showing that the Ordovician infaunalization event left heavy traces in bivalve mitochondrial genomes.

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“…We also confirmed the previously noted variability of bivalve residue 43 of the same gene (Degli Esposti 2015; fig. 3), which is also part of the Q reacting chamber (Baradaran et al.…”

Section: Discussionsupporting

confidence: 92%

“…Menaquinone is the dominant membrane Q in some prokaryotes, like gram-positive bacteria (Degli Esposti 2015); plastoquinone is the typical membrane Q of cyanobacteria (Battchikova et al. 2011).…”

Section: Introductionmentioning

confidence: 99%

Burrowers from the Past: Mitochondrial Signatures of Ordovician Bivalve Infaunalization

Plazzi

Puccio

Passamonti

2017

Genome Biology and Evolution

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“…[ 31 – 34 ]). The eukaryotic orthologs of these proteins are the 24 and 51 kDa subunits of mitochondrial complex I that are always coded by nuclear DNA, while the rest of complex I subunits is encoded by mtDNA in several protists [ 5 , 32 , 34 ]. The same proteins are found in the hydrogenosomes - a specialised form of MRO [ 19 ] - of Trichomonas [ 11 ] and Sawyeria , an anaerobic Heterolobosea [ 35 ], which lack complex I [ 19 ].…”

Section: Resultsmentioning

confidence: 99%

“…The gene cluster containing the long form of [FeFe]-hydrogenase and NuoEF homologues in the organisms identified from metagenomic analysis [ 20 ] resembles the hymABC operon described in Clostridiales [ 36 , 37 ] (Table 1 ). In turn, this operon clearly derives from the Fds operon of NAD-dependent formate dehydrogenase [ 38 ], from which the NADH-reacting module of respiratory complex I originated [ 32 , 34 ]. Of note, the genome of the abovementioned metagenomic α proteobacteria invariably contains the gene for Pyruvate:Ferredoxin Oxidoreductase (PFO, Table 1 ), a key enzyme in the anaerobic metabolism of Clostridiales [ 36 , 37 ] and also anaerobic eukaryotes [ 19 ].…”

Section: Resultsmentioning

confidence: 99%

Alpha proteobacterial ancestry of the [Fe-Fe]-hydrogenases in anaerobic eukaryotes

et al. 2016

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Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to α proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic α proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba. These enzymes are thought to derive from bacterial lineages other than α proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that α proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an α proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes.Reviewers: This article was reviewed by William Martin and Nick Lane, both suggested by the Authors.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-016-0136-3) contains supplementary material, which is available to authorized users.

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“…As discussed in the introduction, genomes of Nautilia profundicola and Caminibacter mediatlanticus (the deepest-branching Epsilonproteobacteria (Zhang and Sievert, 2014)) as well as several Lebetimonas isolates (Meyer and Huber 2013) show that these organisms all possess this incomplete form of complex I as well as "energy-conserving hydrogenases" (Ech; Hedderich, 2004). Ech, which couple hydrogen oxidation to ferredoxin reduction, also lack NuoEFG subunits and are thought to be the evolutionary precursor of complex I (Hedderich, 2004 Epsilonproteobacteria contain what is thought to be the most ancestral forms of complex I (Esposti, 2016), investigations into the functions of these enzymes in both deep-and shallowbranching Epsilonproteobacteria will shed light on the evolution of this core bioenergetic enzyme complex. As discussed in Chapter 4, this evolutionary change likely has to do with their adaptive radiation from hydrothermal environments into more oxic environments that appeared during the oxygenation of ancient Earth.…”

Section: Genome Scale Metabolic Modelingmentioning

confidence: 99%

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

McNichol¹

2016

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Chemoautotrophic ecosystems at deep-sea hydrothermal vents were discovered in 1977, but not until 1995 were free-living autotrophic Epsilonproteobacteria identified as important microbial community members. Because the deep-sea is food-starved, the autotrophic metabolism of hydrothermal vent Epsilonproteobacteria may be very important for deep-sea consumers. However, quantifying their metabolic activities in situ has remained difficult, and biochemical mechanisms underlying their autotrophic physiology are poorly described. To gain insight into environmental processes, an approach was developed for incubations of microbes at in situ pressure and temperature (25 MPa, 24 o C) with various combinations of electron donors/acceptors (H 2 , O 2 and NO 3 -and 13 HCO 3 -) as a tracer to track carbon fixation. During short (18-24 h) incubations of low-temperature vent fluids from Crab Spa (9 o N East Pacific Rise), the concentration of electron donors/acceptors and cell numbers were monitored to quantify microbial processes. Measured rates were generally higher than previous studies, and the stoichiometry of microbially-catalyzed redox reactions revealed new insights into sulfur and nitrogen cycling. Single-cell, taxonomically-resolved tracer incorporation showed Epsilonproteobacteria dominated carbon fixation, and their growth efficiency was calculated based on electron acceptor consumption. Using these data, in situ primary productivity, microbial standing stock, and average biomass residence time of the deep-sea vent subseafloor biosphere were estimated. Finally, the population structures of the most abundant genera Sulfurimonas and Thioreductor were shown to be strongly influenced by pO 2 and temperature respectively, providing a mechanism for niche differentiation in situ. To gain insights into the core biochemical reactions underlying autotrophy in Epsilonprotebacteria, a theoretical metabolic model of Sulfurimonas denitrificans was developed. Validated iteratively by comparing in silico yields with data from chemostat experiments, the model generated hypotheses explaining critical, yet so far unresolved reactions supporting chemoautotrophy in Epsilonproteobacteria. For example, it provides insight into how energy is conserved during sulfur oxidation coupled to denitrification, how reverse electron transport produces ferredoxin for carbon fixation, and why aerobic growth yields are only slightly higher compared to denitrification. As a whole, this thesis provides important contributions towards understanding core mechanisms of chemoautrophy, as well as the in situ productivity, physiology and ecology of autotrophic Epsilonproteobacteria.

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Genome Analysis of Structure–Function Relationships in Respiratory Complex I, an Ancient Bioenergetic Enzyme

Cited by 17 publications

References 118 publications

Burrowers from the Past: Mitochondrial Signatures of Ordovician Bivalve Infaunalization

Burrowers from the Past: Mitochondrial Signatures of Ordovician Bivalve Infaunalization

Alpha proteobacterial ancestry of the [Fe-Fe]-hydrogenases in anaerobic eukaryotes

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

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