Nectar-feeding bats and birds show parallel molecular adaptations in sugar metabolism enzymes

Potter, Joshua H.T.; Drinkwater, Rosie; Davies, Kalina T. J.; Nesi, Nicolas; Lim, Marisa; Yohe, Laurel; Chi, Hai; Zhang, Xiaoqing; Lim, Burton K.; Witt, Christopher C.; Tsagkogeorga, Georgia; Reis, Mario dos; Liu, Yang; Furey, W.; Whitley, Matthew J.; Aksentijević, Dunja; Dávalos, Liliana M.; Rossiter, Stephen J.

doi:10.1016/j.cub.2021.08.018

Cited by 10 publications

(14 citation statements)

References 74 publications

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“…Whereas signatures of selection in more broadly expressed glycolytic enzymes, detected here and previously ( 10 ), highlight additional genomic changes with relevance for systemic metabolic adaptations in hummingbirds, metabolic shifts caused by losing the muscle-expressed FBP2 gene were likely restricted to muscle tissue. Because down-regulation or inactivation of FBP2 provides a mechanism to increase metabolic capacity in muscle by up-regulating sugar metabolism, the loss of the FBP2 gene was likely beneficial for hummingbirds and could have been a key step in the coevolution of nectarivory and energy-demanding hovering flight.…”

Section: Discussionsupporting

confidence: 54%

“…S12). Notably, ALDOB and PDHB also evolved under positive selection in nectar-feeding bats ( 10 ). Finally, compared to swift, expression of ALDOB and ENO1 is significantly up-regulated in hummingbird liver and expression of PDHA2 and PDHB is significantly up-regulated in hummingbird muscle and liver (Fig.…”

Section: Glycolytic Genes Evolved Under Positive Selectionmentioning

confidence: 99%

“…Hummingbirds have the distinctive ability to directly metabolize dietary fructose as efficiently as glucose ( 7 , 8 ), and their sweet taste perception evolved by co-option of an umami taste receptor ( 9 ). Sequence analyses revealed signatures of positive selection in hummingbird glycolytic enzymes ( 10 ). However, the genomic basis of metabolic muscle adaptations in hummingbirds is largely unknown.…”

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confidence: 99%

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Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Osipova

Barsacchi

Brown

et al. 2023

Science

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Hummingbirds possess distinct metabolic adaptations to fuel their energy-demanding hovering flight, but the underlying genomic changes are largely unknown. Here, we generated a chromosome-level genome assembly of the long-tailed hermit and screened for genes that have been specifically inactivated in the ancestral hummingbird lineage. We discovered that FBP2 (fructose-bisphosphatase 2), which encodes a gluconeogenic muscle enzyme, was lost during a time period when hovering flight evolved. We show that FBP2 knockdown in an avian muscle cell line up-regulates glycolysis and enhances mitochondrial respiration, coincident with an increased mitochondria number. Furthermore, genes involved in mitochondrial respiration and organization have up-regulated expression in hummingbird flight muscle. Together, these results suggest that FBP2 loss was likely a key step in the evolution of metabolic muscle adaptations required for true hovering flight.

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Section: Discussionsupporting

confidence: 54%

Section: Glycolytic Genes Evolved Under Positive Selectionmentioning

confidence: 99%

mentioning

confidence: 99%

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Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Osipova

Barsacchi

Brown

et al. 2023

Science

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“…High glucose level in the body also affects the expression of Q91Y97 protein (gene Aldob), which can further affect glycolysis gluconeogenesis, pentose phosphate pathway and tricarboxylic acid (TCA) cycle ( Zhou et al, 2020 ; Potter et al, 2021 ). Q91Y97 protein is involved in step of the subpathway that synthesizes D-glyceraldehyde 3-phosphate and glycerone phosphate from D-glucose.…”

Section: Discussionmentioning

confidence: 99%

Multi-omics analysis reveals the pathogenesis of db/db mice diabetic kidney disease and the treatment mechanisms of multi-bioactive compounds combination from Salvia miltiorrhiza

Xiang²,

Su³

et al. 2022

Front. Pharmacol.

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Diabetic kidney disease (DKD) is a common diabetic complication. Salvia miltiorrhiza has significant therapeutic effects on diabetes complications, although the mechanism remains unclear. Here, biochemical indicators and pathological changes were used to screen out the optimal Salvia miltiorrhiza multi-bioactive compounds combination. Metabolomics, transcriptomics and proteomics were used to explore the pathogenesis of DKD. RT-PCR and parallel reaction monitoring targeted quantitative proteome analysis were utilized to investigate treatment mechanisms of the optimal Salvia miltiorrhiza multi-bioactive compounds combination. The db/db mice showed biochemical abnormalities and renal lesions. The possible metabolic pathways were steroid hormone biosynthesis and sphingolipid metabolism. The 727 differential genes found in transcriptomics were associated with biochemical indicators via gene network to finally screen 11 differential genes, which were mainly key genes of TGF-β/Smad and PI3K/Akt/FoxO signaling pathways. Salvia miltiorrhiza multi-bioactive compounds combination could significantly regulate the Egr1, Pik3r3 and Col1a1 genes. 11 differentially expressed proteins involved in the two pathways were selected, of which 9 were significantly altered in db/db mice compared to db/m mice. Salvia miltiorrhiza multi-bioactive compounds combination could callback Q9DBM2, S4R1W1, Q91Y97, P47738, A8DUK4, and A2ARV4. In summary, Salvia miltiorrhiza multi-bioactive compounds combination may ameliorate kidney injury in diabetes through regulation of TGF-β/Smad and PI3K/Akt/FoxO signaling pathways.

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“…Diet is one key requirement for survival of any species and the quest to acquire and digest nutrients can lead to the evolution of physiological and morphological traits by posing strong selection pressures on the organism (Hecker et al 2019 ; Román‐Palacios et al 2019 ). Bats exhibit unparalleled diversity in food habits ranging from feeding on blood to consuming fruits, nectar, insects, and small vertebrates (Potter et al 2021a and b ). Their diverse food habits are associated with similar diversity in physiological adaptations as well as genomics changes (Fig.…”

Section: Introductionmentioning

confidence: 99%

Next Generation Sequencing Revolutionizes Organismal Biology Research in Bats

et al. 2023

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The advent of next generation sequencing technologies (NGS) has greatly accelerated our understanding of critical aspects of organismal biology from non-model organisms. Bats form a particularly interesting group in this regard, as genomic data have helped unearth a vast spectrum of idiosyncrasies in bat genomes associated with bat biology, physiology, and evolution. Bats are important bioindicators and are keystone species to many eco-systems. They often live in proximity to humans and are frequently associated with emerging infectious diseases, including the COVID-19 pandemic. Nearly four dozen bat genomes have been published to date, ranging from drafts to chromosomal level assemblies. Genomic investigations in bats have also become critical towards our understanding of disease biology and host–pathogen coevolution. In addition to whole genome sequencing, low coverage genomic data like reduced representation libraries, resequencing data, etc. have contributed significantly towards our understanding of the evolution of natural populations, and their responses to climatic and anthropogenic perturbations. In this review, we discuss how genomic data have enhanced our understanding of physiological adaptations in bats (particularly related to ageing, immunity, diet, etc.), pathogen discovery, and host pathogen co-evolution. In comparison, the application of NGS towards population genomics, conservation, biodiversity assessment, and functional genomics has been appreciably slower. We reviewed the current areas of focus, identifying emerging topical research directions and providing a roadmap for future genomic studies in bats.

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Nectar-feeding bats and birds show parallel molecular adaptations in sugar metabolism enzymes

Cited by 10 publications

References 74 publications

Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Loss of a gluconeogenic muscle enzyme contributed to adaptive metabolic traits in hummingbirds

Multi-omics analysis reveals the pathogenesis of db/db mice diabetic kidney disease and the treatment mechanisms of multi-bioactive compounds combination from Salvia miltiorrhiza

Next Generation Sequencing Revolutionizes Organismal Biology Research in Bats

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