Genomic and transcriptomic analyses of Heteropoda venatoria reveal the expansion of P450 family for starvation resistance in spider
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Abstract
Background
Spiders generally exhibit robust starvation resistance, with hunting spiders, represented by Heteropoda venatoria , being particularly outstanding in this regard. Given the challenges posed by climate change and habitat fragmentation, understanding how spiders adjust their physiology and behavior to adapt to the uncertainty of food resources is crucial for predicting ecosystem responses and adaptability.
Results
We sequenced the genome of H. venatoria and, through comparative genomic analysis, discovered significant expansions in gene families related to lipid metabolism, such as cytochrome P450 and steroid hormone biosynthesis genes. We also systematically analyzed the gene expression characteristics of H. venatoria at different starvation resistance stages and found that the fat body plays a crucial role during starvation in spiders. This study indicates that during the early stages of starvation, H. venatoria relies on glucose metabolism to meet its energy demands. In the middle stage, gene expression stabilizes, whereas in the late stage of starvation, pathways for fatty acid metabolism and protein degradation are significantly activated, and autophagy is increased, serving as a survival strategy under extreme starvation. Additionally, analysis of expanded P450 gene families revealed that H. venatoria has many duplicated CYP3 clan genes that are highly expressed in the fat body, which may help maintain a low-energy metabolic state, allowing H. venatoria to endure longer periods of starvation. We also observed that the motifs of P450 families in H. venatoria are less conserved than those in insects, which may be related to the greater polymorphism of spider genomes.
Conclusions
This research not only provides important genetic and transcriptomic evidence for understanding the starvation mechanisms of spiders but also offers new insights into the adaptive evolution of arthropods.
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AbstractBackground Spiders generally exhibit robust starvation resistance, with hunting spiders, represented by Heteropoda venatoria, being particularly outstanding in this regard. Given the challenges posed by climate change and habitat fragmentation, understanding how spiders adjust their physiology and behavior to adapt to the uncertainty of food resources is crucial for predicting ecosystem responses and adaptability.Results We sequenced the genome of H. venatoria and, through comparative genomic analysis, discovered significant expansions in gene families related to lipid metabolism, such as cytochrome P450 and steroid hormone biosynthesis genes. We also systematically analyzed the gene expression characteristics of H. venatoria at different starvation resistance stages and found that the fat body plays a crucial role during …
AbstractBackground Spiders generally exhibit robust starvation resistance, with hunting spiders, represented by Heteropoda venatoria, being particularly outstanding in this regard. Given the challenges posed by climate change and habitat fragmentation, understanding how spiders adjust their physiology and behavior to adapt to the uncertainty of food resources is crucial for predicting ecosystem responses and adaptability.Results We sequenced the genome of H. venatoria and, through comparative genomic analysis, discovered significant expansions in gene families related to lipid metabolism, such as cytochrome P450 and steroid hormone biosynthesis genes. We also systematically analyzed the gene expression characteristics of H. venatoria at different starvation resistance stages and found that the fat body plays a crucial role during starvation in spiders. This study indicates that during the early stages of starvation, H. venatoria relies on glucose metabolism to meet its energy demands. In the middle stage, gene expression stabilizes, whereas in the late stage of starvation, pathways for fatty acid metabolism and protein degradation are significantly activated, and autophagy is increased, serving as a survival strategy under extreme starvation. Additionally, analysis of expanded P450 gene families revealed that H. venatoria has many duplicated CYP3 clan genes that are highly expressed in the fat body, which may help maintain a low-energy metabolic state, allowing H. venatoria to endure longer periods of starvation. We also observed that the motifs of P450 families in H. venatoria are less conserved than those in insects, which may be related to the greater polymorphism of spider genomes.Conclusions This research not only provides important genetic and transcriptomic evidence for understanding the starvation mechanisms of spiders but also offers new insights into the adaptive evolution of arthropods.
This work has been peer reviewed in GigaScience (https://doi.org/10.1093/gigascience/giaf019), which carries out open, named peer-review. These reviews are published under a CC-BY 4.0 license and were as follows:
Reviewer 2: Sandra Correa-Garhwal
The manuscript "Genomic and transcriptomic analyses of Heteropoda venatoria reveal the expansion of P450 family for starvation resistance in spider" uses comparative genomics to study the underlying mechanisms of starvation resistance. I appreciate that the authors have produced a high-quality genome for an RTA species. The methods are sound and some interesting gene families are highlighted as key factors in starvation resistance.
One primary concern I have relates to the study's setup and hypothesis. As currently written, the study comes across as a fishing expedition rather than a focused research project. Although the introduction is informative, it lacks a clear rationale for including this particular species. The reasoning only becomes apparent at the end of the gene family expansion and contraction section. Additionally, I am unsure if being an active hunter makes feeding more unpredictable compared to web-based prey capture. I recommend incorporating this information into the introductory paragraph to better establish the context for the analysis. While terms like "autophagy" and "energy homeostasis" are appropriate for a scientific audience, consider briefly defining them for clarity, especially if the intended audience might not be familiar with all the terminology. Although authors mention that there is no high-quality genome sequence for H. venatoria, it could be helpful to elaborate on why this is significant for understanding starvation resistance. A brief explanation of how genomic data could enhance understanding of the molecular mechanisms involved would strengthen this point. The conclusion provides a clear goal for your study, but it could be more impactful. You might want to emphasize the broader implications of your research findings for ecological conservation and biodiversity. End with a statement about the importance of understanding these mechanisms in the context of preserving ecosystems and addressing challenges posed by climate change.
For the discussion, while the content is detailed, some parts feel slightly repetitive or could be more concise. For instance, the description of P450 gene expression could be streamlined by removing redundant mentions of their role in metabolic rate regulation. Example: In the discussion section "Interestingly, we found that some P450 families are expanded in H. venatoria, and most P450 genes are more highly expressed in the fat body than in other tissues…" This point is later reiterated in the sentence about other spider species. These ideas could be combined for efficiency. The paragraph about the phylogenetic analysis of the CYP3 clan could be shortened. While it is an interesting finding, some of the details (like the number of genes or proteins) might be better suited for the main text rather than a summary. Focusing more on the functional implications of these duplications would keep the reader engaged. Though the findings are well-explained, the broader significance could be emphasized more explicitly. For example, why is understanding these mechanisms important for the field of arachnid biology, evolutionary biology, or even practical applications (e.g., pest control, conservation)? You could add a closing sentence that ties everything together and highlights the broader relevance of the findings, such as the evolutionary or ecological importance of these adaptations in spiders.
Other comments: Last paragraph of the introduction: When introducing Heteropoda venatoria, please spell out the species name the first time that is used. The sentence "However, these findings indicate that H. venatoria does not feed in a stable manner and often experiences periods of starvation." Does not fit the rest of the text. Finding from what study? Transcription design for starvation resistance in H. venatoria section: First sentence: What samples? confusing to start like this. Please add information about the samples. You could delete "the samples of H. venatoria were subjected to" it will read better. Are all 23 CYP# clan genes on chromosome 4 tandemly arrayed? Figure 4 - add more information about the figure. For pannel C, What do the red lines show? Grey? Numbers in the circles? While I know what they represent, other readers might not. The finding that H. venatoria chromosomes have undergone lots of chromosomal fragmentation is very interesting, and it is clearly shown on the figure. Which is why I think that more detail is needed. In this sentence "In Uloborus diversus, members of this subfamily are located on Chr5 and an unanchored scaffold." You need to specify which members. Figure 5 - Include a description of the tissues. What is Epi? Ducts? Tail?
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AbstractBackground Spiders generally exhibit robust starvation resistance, with hunting spiders, represented by Heteropoda venatoria, being particularly outstanding in this regard. Given the challenges posed by climate change and habitat fragmentation, understanding how spiders adjust their physiology and behavior to adapt to the uncertainty of food resources is crucial for predicting ecosystem responses and adaptability.Results We sequenced the genome of H. venatoria and, through comparative genomic analysis, discovered significant expansions in gene families related to lipid metabolism, such as cytochrome P450 and steroid hormone biosynthesis genes. We also systematically analyzed the gene expression characteristics of H. venatoria at different starvation resistance stages and found that the fat body plays a crucial role during …
AbstractBackground Spiders generally exhibit robust starvation resistance, with hunting spiders, represented by Heteropoda venatoria, being particularly outstanding in this regard. Given the challenges posed by climate change and habitat fragmentation, understanding how spiders adjust their physiology and behavior to adapt to the uncertainty of food resources is crucial for predicting ecosystem responses and adaptability.Results We sequenced the genome of H. venatoria and, through comparative genomic analysis, discovered significant expansions in gene families related to lipid metabolism, such as cytochrome P450 and steroid hormone biosynthesis genes. We also systematically analyzed the gene expression characteristics of H. venatoria at different starvation resistance stages and found that the fat body plays a crucial role during starvation in spiders. This study indicates that during the early stages of starvation, H. venatoria relies on glucose metabolism to meet its energy demands. In the middle stage, gene expression stabilizes, whereas in the late stage of starvation, pathways for fatty acid metabolism and protein degradation are significantly activated, and autophagy is increased, serving as a survival strategy under extreme starvation. Additionally, analysis of expanded P450 gene families revealed that H. venatoria has many duplicated CYP3 clan genes that are highly expressed in the fat body, which may help maintain a low-energy metabolic state, allowing H. venatoria to endure longer periods of starvation. We also observed that the motifs of P450 families in H. venatoria are less conserved than those in insects, which may be related to the greater polymorphism of spider genomes.Conclusions This research not only provides important genetic and transcriptomic evidence for understanding the starvation mechanisms of spiders but also offers new insights into the adaptive evolution of arthropods.
This work has been peer reviewed in GigaScience (https://doi.org/10.1093/gigascience/giaf019), which carries out open, named peer-review. These reviews are published under a CC-BY 4.0 license and were as follows:
Reviewer 1: Hui Xiang
In this study, the authors deciphered the chromosome-level genome of a RTA spider Heteropoda venatoria with large body size and generated comprehensive comparative transcriptomes of fat body and whole body among CK and starvation status. Generally, this study added important genomic and transcriptomic data of spiders and provided some cues in understanding the molecular changes during starvation. However, the organization of the manuscript is quite problematic.
- As to the Results section, please be concise and highlight the main results，avoiding accumulating complex results. Do not present too many statements in terms of introduction and discussion in Results. Do not raise too many hypotheses in the results.
- As for the involvement of the Hippo signaling pathway in lipid metabolism regulation, the cited literature and mentioned genes are not related to the results of this study. As for the analysis of P450 results, the descriptions of structural analysis are quite complex and difficult to understand. The authors did not explain clearly the relationship between the expansion of P450 genes and hunger resistance in the results of this study.
- The author's analyses of DEG enrichment results in transcriptome analysis is confusing. Firstly,I can't agree with the authors in that "During the early stage of starvation (from CK to 2 W), many genes, specifically those involved in oxidative phosphorylation and thermogenesis pathways, were up-regulated (Fig. 2E). These findings indicate that during the early starvation stage, energy metabolism in H. venatoria occurs regularly, with sufficient supply of energy." There are a batch of DEGs between 2W and CK, and a lot of pathways involved in neurodegeneration related pathways. How to explain these changes? Secondly, as to 4W to 8W, I can not understand the relationship of down-regulation of hippo signaling pathway to the authors' speculation that "H. venatoria may reduce its cellular glucose uptake and utilization to adjust to the food-scarce environment.", as this pathway involved in lipid metabolism, as the authors stated. Thirdly, from 14 W to 19 W, pathways such Lysosome and apoptosis were down-regulated instead of up-regulated. So how the authors thought autophagy became more active?
- "We speculate that during the evolution of spider genomes, two types of repeat sequences, TcMar and LTR sequences, had a significant impact on the size of spider genomes. Interestingly, we found that in H. venatoria chromosomes, regions with a high proportion of repeats also presented an increase in GC content (Fig. 1B)" The author's conclusion that high repeat region has higher CG content is based on Fig1B alone, which is too arbitrary. They needs more solid evidence and more detailed analysis. For example, the GC content of TE region could be compared with that of whole genome, and the GC content of gene region. The significance of the relevant results should be explained. In addition, the author should make a more convincing discussion of this result based on the more literature.
- "We gathered genomic data and annotations for one scorpion and seven chromosome-level spider genomes using the scorpion as an outgroup [35-42]"。Many spider genomes have been published at the chromosomal level. What were the principles behind the spider genomes the authors selected in this study?
- "Transcriptome design for starvation resistance in H. venatoria" in Results should be partially moved Methods and here the authors should straightforwardly highlighted the results .
- I can't understand the significance of Fig 2C. The authors did not explain it in the manuscript, either.
- "The PCA results from both the fat body and whole-body transcriptomes indicated that H. venatoria transcriptome at 19 weeks of starvation was markedly distinct from that at other stages (Fig. 2A, B). Consequently, we conducted a differential analysis of the transcriptome at 19 weeks." Please clarify how the comparative transcriptomes were conducted for differential analysis.
- The language should be polished.
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