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Gut Microbiota of Drosophila subobscura Contributes to Its Heat Tolerance and Is Sensitive to Transient Thermal Stress.

ABSTRACT: The gut microbiota can contribute to host physiology leading to an increase of resistance to abiotic stress conditions. For instance, temperature has profound effects on ectotherms, and the role of the gut microbiota on the thermal tolerance of ectotherms is a matter of recent research. However, most of these studies have been focused on single static temperatures instead of evaluating thermal tolerance in a wide range of stressful temperatures. Additionally, there is evidence supporting that the gut microbiota is sensitive to environmental temperature, which induces changes in its composition and diversity. These studies have evaluated the effects of thermal acclimation (>2 weeks) on the gut microbiota, but we know little about the impact of transient thermal stress on the composition and diversity of the gut microbiota. Thus, we investigated the role of the gut microbiota on the heat tolerance of Drosophila subobscura by measuring the heat tolerance of conventional and axenic flies exposed to different heat stressful temperatures (35, 36, 37, and 38°C) and estimating the heat tolerance landscape for both microbiota treatments. Conventional flies exposed to mild heat conditions exhibited higher thermal tolerance than axenic flies, whereas at higher stressful temperatures there were no differences between axenic and conventional flies. We also assessed the impact of transient heat stress on the taxonomical abundance, diversity, and community structure of the gut microbiota, comparing non-stressed flies (exposed to 21°C) and heat-stressed flies (exposed to 34°C) from both sexes. Bacterial diversity indices, bacterial abundances, and community structure changed between non-stressed and heat-stressed flies, and this response was sex-dependent. In general, our findings provide evidence that the gut microbiota influences heat tolerance and that heat stress modifies the gut microbiota at the taxonomical and structural levels. These results demonstrate that the gut microbiota contributes to heat tolerance and is also highly sensitive to transient heat stress, which could have important consequences on host fitness, population risk extinction, and the vulnerability of ectotherms to current and future climatic conditions.

SUBMITTER: Jaramillo A

PROVIDER: S-EPMC8137359 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundDespite its pervasiveness, the genetic basis of adaptation resulting in variation directly or indirectly related to temperature (climatic) gradients is poorly understood. By using 3-fold replicated laboratory thermal stocks covering much of the physiologically tolerable temperature range for the temperate (i.e., cold tolerant) species Drosophila subobscura we have assessed whole-genome transcriptional responses after three years of thermal adaptation, when the populations had already diverged for inversion frequencies, pre-adult life history components, and morphological traits. Total mRNA from each population was compared to a reference pool mRNA in a standard, highly replicated two-colour competitive hybridization experiment using cDNA microarrays.ResultsA total of 306 (6.6%) cDNA clones were identified as 'differentially expressed' (following a false discovery rate correction) after contrasting the two furthest apart thermal selection regimes (i.e., 13 degrees C vs . 22 degrees C), also including four previously reported candidate genes for thermotolerance in Drosophila (Hsp26, Hsp68, Fst, and Treh). On the other hand, correlated patterns of gene expression were similar in cold- and warm-adapted populations. Analysis of functional categories defined by the Gene Ontology project point to an overrepresentation of genes involved in carbohydrate metabolism, nucleic acids metabolism and regulation of transcription among other categories. Although the location of differently expressed genes was approximately at random with respect to chromosomes, a physical mapping of 88 probes to the polytene chromosomes of D. subobscura has shown that a larger than expected number mapped inside inverted chromosomal segments.ConclusionOur data suggest that a sizeable number of genes appear to be involved in thermal adaptation in Drosophila, with a substantial fraction implicated in metabolism. This apparently illustrates the formidable challenge to understanding the adaptive evolution of complex trait variation. Furthermore, some clustering of genes within inverted chromosomal sections was detected. Disentangling the effects of inversions will be obviously required in any future approach if we want to identify the relevant candidate genes.

Project description:BackgroundThe role of chromosomal arrangements in adaptation is supported by the repeatable clinal variation in inversion frequencies across continents in colonizing species such as Drosophila subobscura. However, there is a lack of knowledge on the genetic variation in genes within inversions, possibly targets of climatic selection, across a geographic latitudinal gradient. In the present study we analysed four candidate loci for thermal adaptation, located close to the breakpoints, in two chromosomal arrangements of the sex (A) chromosome of Drosophila subobscura with different thermal preferences. Individual chromosomes with A2 (the inverted arrangement considered warm adapted) or AST (the standard ancestral arrangement considered cold adapted) were sequenced across four European localities at varying latitudes, up to ~ 2500 Kms apart.ResultsImportantly, we found very low differentiation for each specific arrangement across populations as well as no clinal patterns of genomic variation. This suggests wide gene exchange along the cline. Differentiation between the sex chromosome arrangements was significant in the two more proximal regions relative to the AST orientation but not in the distal ones, independently of their location inside or outside the inversion. This can be possibly due to variation in the levels of gene flux and/or selection acting in these regions.ConclusionsGene flow appears to have homogenized the genetic content within-arrangement at a wide geographical scale, despite the expected diverse selective pressures in the specific natural environments of the different populations sampled. It is thus likely that the inversion frequency clines in this species are being maintained by local adaptation in face of gene flow. The differences between arrangements at non-coding regions might be associated with the previously observed differential gene expression in different thermal regimes. Higher resolution genomic scans for individual chromosomal arrangements performed over a large environmental gradient are needed to find the targets of selection and further elucidate the adaptive mechanisms maintaining chromosomal inversion polymorphisms.

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Gut Microbiota of Drosophila subobscura Contributes to Its Heat Tolerance and Is Sensitive to Transient Thermal Stress.

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