The archaeal LDH-like malate dehydrogenase from Ignicoccus islandicus displays dual substrate recognition, hidden allostery and a non-canonical tetrameric oligomeric organization

Roche, J; Girard, Éric; Mas, Caroline; Madern, Dominique

doi:10.1016/j.jsb.2019.07.006

Cited by 19 publications

(18 citation statements)

References 71 publications

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“…Alternatively, the lactate dehydrogenase-like malate dehydrogenase homologs found in AOA possess features indicating that they could have a broad substrate specificity, being able to utilize pyruvate in addition to oxaloacetate, and producing the L-stereoisomers of the products (see Supplementary Information and Figs. S5 and S6 ), with the concomitant reduction of NAD + [ 81 ].…”

Section: Resultsmentioning

confidence: 99%

Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages

et al. 2021

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Marine sediments represent a vast habitat for complex microbiomes. Among these, ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are one of the most common, yet little explored, inhabitants, which seem extraordinarily well adapted to the harsh conditions of the subsurface biosphere. We present 11 metagenome-assembled genomes of the most abundant AOA clades from sediment cores obtained from the Atlantic Mid-Ocean ridge flanks and Pacific abyssal plains. Their phylogenomic placement reveals three independently evolved clades within the order Nitrosopumilales, of which no cultured representative is known yet. In addition to the gene sets for ammonia oxidation and carbon fixation known from other AOA, all genomes encode an extended capacity for the conversion of fermentation products that can be channeled into the central carbon metabolism, as well as uptake of amino acids probably for protein maintenance or as an ammonia source. Two lineages encode an additional (V-type) ATPase and a large repertoire of DNA repair systems that may allow to overcome the challenges of high hydrostatic pressure. We suggest that the adaptive radiation of AOA into marine sediments occurred more than once in evolution and resulted in three distinct lineages with particular adaptations to this extremely energy-limiting and high-pressure environment.

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Section: Resultsmentioning

confidence: 99%

Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages

et al. 2021

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“…On the contrary, eukaryotic LDHs and MDHs are considered non-allosteric. The divergence from a common ancestral gene, and the presence of allosteric and non-allosteric enzymes in the super-family make LDH-like MDHs and LDHs a perfect model to investigate the evolutionary emergence of allostery as a mechanism of functional regulation [20][21][22] . In a previous work based on the combination of neutron scattering experiments and molecular simulations, it was shown that the non-allosteric LDH from rabbit uses temperature to reorganize its catalytic site in a similar manner as allosteric LDHs do upon co-factor binding, and changing from the apo to holo state 23 .…”

Section: Introductionmentioning

confidence: 99%

“…In a previous work based on the combination of neutron scattering experiments and molecular simulations, it was shown that the non-allosteric LDH from rabbit uses temperature to reorganize its catalytic site in a similar manner as allosteric LDHs do upon co-factor binding, and changing from the apo to holo state 23 . More recently, a biochemical and structural study using a LDH-like MDH from a hyperthermophilic archaea has revealed that this enzyme, which was considered as non-allosteric, may exhibit a homotropic activation capacity in certain conditions 21 .…”

Section: Introductionmentioning

confidence: 99%

Temperature Unmasks Allosteric Propensity in a Thermophilic Malate Dehydrogenase via Dewetting and Collapse

et al. 2020

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In this work we combine experiments and molecular simulations to unveil the hidden allosteric propensity of a thermophilic malate dehydrogenase protein (MDH). We provide evidence that at its working temperature the non-allosteric MDH takes a compact structure because of internal dewetting, and reorganizes the active state toward functional conformations similarly to its homologous allosteric LDHs. Moreover, a single-point mutation confers the MDH a cooperative behaviour that mimics an allosteric LDH. Our work not only demonstrates that thermophilic MDHs use temperature as an external parameter to regulate its functionality in a similar way allosteric LDHs use substrates/cofactors binding, but also shows that the scaffold of MDHs possesses an intrinsic and hidden allosteric potentiality.

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“…Alternatively, the lactate dehydrogenaselike malate dehydrogenase homologs found in AOA possess features indicating that they could have a broad substrate specificity, being able to utilize pyruvate in addition to oxaloacetate, and producing the L-stereoisomers of the products (see Supplementary Information and Fig. S5), with the concomitant reduction of NAD + [78].…”

Section: Utilization Of Exogenous Organic Compoundsmentioning

confidence: 99%

Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages

Kerou

Ponce‐Toledo

Zhao

et al. 2020

Preprint

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26Marine sediments represent a vast habitat for complex microbiomes. Among these, ammonia oxidizing 27 archaea (AOA) of the phylum Thaumarchaeota are one of the most common, yet little explored 28 inhabitants, that seem extraordinarily well adapted to the harsh conditions of the subsurface biosphere. 29We present 11 metagenome-assembled genomes of the most abundant AOA clades from sediment cores 30 obtained from the Atlantic Mid-Ocean ridge flanks and Pacific abyssal plains. Their phylogenomic 31 placement reveals three independently evolved clades within the order Ca. Nitrosopumilales, of which 32 no cultured representative is known yet. In addition to the gene sets for ammonia oxidation and carbon 33 fixation known from other AOA, all genomes encode an extended capacity for the conversion of 34 fermentation products that can be channeled into the central carbon metabolism, as well as uptake of 35 amino acids probably for protein maintenance or as an ammonia source. Two lineages encode an additional (V-type) ATPase and a large repertoire of gene repair systems that may allow to overcome 37 challenges of high hydrostatic pressure. We suggest that the adaptive radiation of AOA into marine 38 sediments occurred more than once in evolution and resulted in three distinct lineages with particular 39 adaptations to this extremely energy limiting and high-pressure environment. 40 41 42 Introduction 43 44 Ammonia oxidizing archaea (AOA) comprise one of the most successful archaeal phyla having 45 colonized almost every imaginable oxic environment of the planet where they emerge as key players in 46 the nitrogen cycle [1-6]. This includes the marine environment where they dominate archaeal 47 communities associated with oxic sediments ranging from shallow estuaries to the open ocean [7-12], 48and from the surface layers all the way into the deep oceanic crust [13][14][15]. In these ecosystems they 49 seem to play a critical role in the transformation of nitrogen compounds and control its partitioning into 50 the bottom ocean and the underlying oceanic crust [12,[14][15][16][17][18][19]). 52Studies from the North Atlantic and Pacific show that the composition of the sedimentary AOA 53 population differs drastically from that in the overlying water suggesting distinct ecophysiological 54 potential to colonise sedimentary environments, albeit all were found to belong to the order 55 Nitrosopumilales (NP) [20]. Whereas the amoA-NP-gamma clade seems to be dominant and 56 omnipresent in these oceans, irrespective of water depths, the amoA-NP-alpha clade represents the most 57 abundant ecotypes in deep ocean waters [6, 7,[21][22][23][24][25][26][27] (nomenclature based amoA gene classification 58 [28]). In contrast, dominant phylotypes in deep-sea sediments belong to the amoA-NP-theta and amoA-59 NP-delta clades [11, 12]. In addition, in cases of oligotrophic oceanic regions, these were detected 60 throughout the sediment column and further into the underlying basaltic crust, even at depth where 61 oxygen is below detection [7, ...

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The archaeal LDH-like malate dehydrogenase from Ignicoccus islandicus displays dual substrate recognition, hidden allostery and a non-canonical tetrameric oligomeric organization

Cited by 19 publications

References 71 publications

Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages

Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages

Temperature Unmasks Allosteric Propensity in a Thermophilic Malate Dehydrogenase via Dewetting and Collapse

Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages

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