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The auxiliary ESCRT complexes provide robustness to cold in poikilothermic organisms.

ABSTRACT: The ESCRT pathway, comprising the in sequence acting ESCRT-0, -I, -II, -III and Vps4 complexes, conducts the abscission of membranes away from the cytosol. Whereas the components of the central ESCRT-III core complex have been thoroughly investigated, the function of the components of the associated two auxiliary ESCRT sub-complexes are not well-understood in metazoans, especially at the organismal level. We here present the developmental analysis of the Drosophila orthologs of the auxiliary ESCRTs Chmp5 and Ist1, DChmp5 and DIst1, which belong to the two auxiliary sub-complexes. While each single null mutant displayed mild defects in development, the Dist1 Dchmp5 double mutant displayed a severe defect, indicating that the two genes act synergistically, but in separate pathways. Moreover, the presented results indicate that the auxiliary ESCRTs provide robustness against cold during development of diverse poikilothermic organisms, probably by preventing the accumulation of the ESCRT-III core component Shrub on the endosomal membrane.

SUBMITTER: Baumers M

PROVIDER: S-EPMC6777356 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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The auxiliary ESCRT complexes provide robustness to cold in poikilothermic organisms.

Bäumers Miriam M Klose Sven S Brüser Christian C Haag Carl C Hänsch Sebastian S Pannen Hendrik H Weidtkamp-Peters Stefanie S Feldbrügge Michael M Klein Thomas T

Biology open 20190902 9

The ESCRT pathway, comprising the in sequence acting ESCRT-0, -I, -II, -III and Vps4 complexes, conducts the abscission of membranes away from the cytosol. Whereas the components of the central ESCRT-III core complex have been thoroughly investigated, the function of the components of the associated two auxiliary ESCRT sub-complexes are not well-understood in metazoans, especially at the organismal level. We here present the developmental analysis of the <i>Drosophila</i> orthologs of the auxili ...[more]

PMID: 31412999

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Project description:Microbial communities experience continuous environmental changes, with temperature fluctuations being the most impacting. This is particularly important considering the ongoing global warming but also in the "simpler" context of seasonal variability of sea-surface temperature. Understanding how microorganisms react at the cellular level can improve our understanding of their possible adaptations to a changing environment. In this work, we investigated the mechanisms through which metabolic homeostasis is maintained in a cold-adapted marine bacterium during growth at temperatures that differ widely (15 and 0°C). We have quantified its intracellular and extracellular central metabolomes together with changes occurring at the transcriptomic level in the same growth conditions. This information was then used to contextualize a genome-scale metabolic reconstruction, and to provide a systemic understanding of cellular adaptation to growth at 2 different temperatures. Our findings indicate a strong metabolic robustness at the level of the main central metabolites, counteracted by a relatively deep transcriptomic reprogramming that includes changes in gene expression of hundreds of metabolic genes. We interpret this as a transcriptomic buffering of cellular metabolism, able to produce overlapping metabolic phenotypes, despite the wide temperature gap. Moreover, we show that metabolic adaptation seems to be mostly played at the level of few key intermediates (e.g., phosphoenolpyruvate) and in the cross talk between the main central metabolic pathways. Overall, our findings reveal a complex interplay at gene expression level that contributes to the robustness/resilience of core metabolism, also promoting the leveraging of state-of-the-art multi-disciplinary approaches to fully comprehend molecular adaptations to environmental fluctuations. IMPORTANCE This manuscript addresses a central and broad interest topic in environmental microbiology, i.e. the effect of growth temperature on microbial cell physiology. We investigated if and how metabolic homeostasis is maintained in a cold-adapted bacterium during growth at temperatures that differ widely and that match measured changes on the field. Our integrative approach revealed an extraordinary robustness of the central metabolome to growth temperature. However, this was counteracted by deep changes at the transcriptional level, and especially in the metabolic part of the transcriptome. This conflictual scenario was interpreted as a transcriptomic buffering of cellular metabolism, and was investigated using genome-scale metabolic modeling. Overall, our findings reveal a complex interplay at gene expression level that contributes to the robustness/resilience of core metabolism, also promoting the use of state-of-the-art multi-disciplinary approaches to fully comprehend molecular adaptations to environmental fluctuations.

Dataset Information

The auxiliary ESCRT complexes provide robustness to cold in poikilothermic organisms.

Publications

The auxiliary ESCRT complexes provide robustness to cold in poikilothermic organisms.

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