1 Introduction

Ascidians, commonly known as sea squirts, are a diverse group of marine invertebrates belonging to the Phylum Chordata, Class Ascidiacea. They play a crucial role in the ecology of marine benthic communities, often forming dense populations on submerged surfaces. Ascidians are found in a variety of marine environments, from shallow coastal waters to the deep sea, and exhibit a wide range of morphological and ecological adaptations (Nydam et al., 2021). The botryllid Ascidians, for instance, include 53 colonial species that thrive in temperate, tropical, and subtropical waters, showcasing their ability to adapt to different environmental conditions.

Understanding the genomic basis of environmental adaptation in Ascidians is essential for several reasons. Firstly, Ascidians occupy a unique evolutionary position at the boundary between invertebrates and vertebrates, making them valuable models for studying evolutionary processes. Secondly, many Ascidian species are invasive, spreading rapidly across the globe and impacting local ecosystems. Investigating the genetic mechanisms underlying their invasive capabilities can provide insights into managing and mitigating their spread (Wei et al., 2020). Additionally, Ascidians harbor diverse microbial communities that are species-specific and tissue-specific, which can have significant implications for their health and ecological interactions (Chen et al., 2016). The study of these microbial associations through genomic approaches can reveal new aspects of symbiosis and microbial ecology (Chen et al., 2016).

This study will explore the genetic and molecular mechanisms that enable sea squirts to thrive in diverse and often challenging marine environments. Covers key findings from recent genomic studies, including the identification of gene families involved in stress response, immune function, and metabolic pathways that contribute to environmental adaptation. The study will provide a valuable resource for researchers interested in evolutionary biology, ecology, and genomics at Scian.

2 Genomic Features of Ascidians

2.1 General structure of ascidian genomes

Ascidians, also known as sea squirts, possess genomes that exhibit unique structural characteristics. The genome of the leathery sea squirt, Styela clava, for instance, is approximately twice the size of that of Ciona intestinalis type A (C. robusta), despite having a comparable number of genes. This expansion is attributed to an increase in transposon number and variation in dominant types (Chen et al., 2020). Additionally, the genomes of Ascidians like Ciona robusta and Ciona savignyi show differences in exon/intron size distributions, which contribute to variations in alternative splicing responses to environmental changes (Huang et al., 2023).

2.2 Unique genomic elements related to adaptation

Ascidians have developed several unique genomic elements that facilitate their adaptation to diverse environments. For example, the genome of Styela clava contains an expanded number of genes encoding heat-shock proteins and members of the complement system (Figure 1), which are crucial for stress responses. Additionally, cold-shock protein genes have been horizontally transferred from bacteria, further aiding in environmental adaptation (Wei et al., 2020). In Ciona robusta, significant genetic differentiation among populations has been observed, with specific loci showing signatures of directional selection in response to local environmental conditions (Lin et al., 2017). Moreover, DNA methylation patterns driven by local environments have been identified, indicating a strong epigenetic component in adaptation (Hoban et al., 2016).

Figure 1 Genome map, gene family and phylogenetic position of Styela clava (Adopted from Wei et al., 2020) Image caption: a, Chromosome-level genome map of S. clava; b, Venn diagram of common and unique gene families among five ascidian species; c, The phylogenetic position, divergence time estimation and gene family analysis of S. clava (Adopted from Wei et al., 2020)

2.3 Comparative genomics: Ascidians and other marine invertebrates

Comparative genomic studies between Ascidians and other marine invertebrates reveal both shared and unique adaptive strategies. For instance, the genetic basis of adaptation in Ascidians shows parallels with other marine organisms, such as the presence of genes under positive selection related to stress responses and environmental tolerance (Valero et al., 2021). However, Ascidians also exhibit distinct features, such as the specific expansion of gene families related to their unique tunic structure and the presence of horizontally transferred genes. Additionally, the genomic landscape of adaptation in Ascidians is shaped by both genetic and epigenetic variations, a feature that is increasingly recognized in other marine invertebrates as well (Guo et al., 2022).

3 Molecular Mechanisms of Environmental Adaptation

3.1 Gene families associated with stress response

Gene families such as heat shock proteins (HSPs) play a crucial role in the stress response of Ascidians. HSPs are highly conserved proteins that assist in protein folding, repair, and protection against stress-induced damage. In the invasive ascidian Ciona savignyi, a comprehensive study identified 32 HSP-related genes, including HSP20, HSP40, HSP60, HSP70, HSP90, and HSP100, which are differentially expressed in response to temperature and salinity challenges (Huang et al., 2018). These proteins help maintain cellular homeostasis under stress conditions by preventing protein misfolding and aggregation. The expansion of HSP gene families, such as HSP70, has also been observed in other Ascidians like Styela clava, suggesting a genomic basis for their broad environmental adaptability (Wei et al., 2020).

3.2 Epigenetic modifications and adaptation

Epigenetic modifications, particularly DNA methylation, are pivotal in the rapid adaptation of Ascidians to environmental changes. In Ciona robusta, significant DNA methylation variations were observed in genes associated with temperature and salinity, such as heat shock protein 90 and Na+-K+-2Cl− cotransporter (Pu and Zhan, 2017). These modifications occur mainly in gene bodies and are correlated with environmental factors, indicating that epigenetic regulation plays a role in local adaptation during biological invasions. Such epigenetic changes can lead to phenotypic plasticity, allowing Ascidians to thrive in diverse and changing environments (Cheaib et al., 2015).

3.3 Transcriptional regulation of adaptation to salinity and temperature

3.3.1 Heat shock proteins and thermal tolerance

Heat shock proteins (HSPs) are central to the thermal tolerance of Ascidians. The transcriptional response of HSP genes to heat stress is well-documented, with HSP70 being one of the most responsive genes. In Ciona savignyi, HSP70-4 showed the highest induction after 1 hour of high-temperature treatment, highlighting its role in thermal adaptation (Huang et al., 2018). The regulation of HSPs involves heat shock transcription factors (HSFs), which bind to heat shock elements (HSEs) in the promoters of HSP genes, initiating their transcription in response to heat stress (Rossoni and Weber, 2019).

3.3.2 Ion Transporters in osmoregulation

Ion transporters are essential for osmoregulation in Ascidians, enabling them to maintain cellular ion balance under varying salinity conditions. The Na+-K+-2Cl− cotransporter, for instance, is crucial for adapting to salinity changes. In Ciona robusta, DNA methylation of this transporter gene was significantly correlated with salinity levels, suggesting that both transcriptional and epigenetic mechanisms regulate its expression. Additionally, in the fish Cynoglossus semilaevis, HSP70 genes were upregulated under low salinity stress, indicating a potential cross-talk between heat shock proteins and ion transporters in osmoregulation (Deng et al., 2021).

4 Genetic Basis of Habitat Specialization

4.1 Adaptation to intertidal and subtidal zones

Ascidians, like many marine organisms, exhibit remarkable adaptations to various environmental conditions, including intertidal and subtidal zones. The leathery sea squirt, Styela clava, provides a compelling example of genomic adaptations that facilitate survival in diverse habitats. The expansion of gene families related to heat-shock proteins and the complement system, as well as the horizontal transfer of cold-shock protein genes, underscores the genetic mechanisms that enable S. clava to thrive in fluctuating thermal environments (Wei et al., 2020). Similarly, the ascidian Pyura chilensis demonstrates significant genetic differentiation across environmental gradients, particularly around the 30 °S transition zone of the Humboldt Current System. This differentiation is driven by adaptive loci correlated with sea surface temperature and other environmental variables, highlighting the role of local adaptation in maintaining genetic structure despite potential gene flow (Segovia et al., 2020).

4.2 Role of horizontal gene transfer in habitat specialization

Horizontal gene transfer (HGT) plays a crucial role in the genomic adaptation of Ascidians to their environments. In Styela clava, the acquisition of cold-shock protein genes from bacteria exemplifies how HGT can introduce novel genetic material that enhances environmental resilience. This genetic exchange allows S. clava to better cope with cold stress, which is particularly advantageous in temperate and polar regions (Valero et al., 2021). The integration of these horizontally transferred genes into the host genome and their subsequent functional assimilation illustrate the dynamic nature of ascidian genomes in response to environmental pressures (Li, 2024).

4.3 Case study: genomic insights from polar and tropical Ascidians

The study of Ascidians from polar and tropical regions provides valuable insights into the genomic basis of environmental adaptation. For instance, the genomic analysis of Styela clava reveals significant expansions in gene families associated with stress responses, which are critical for survival in both cold polar waters and warmer temperate zones (Feng et al., 2021). Additionally, the research on Pyura chilensis along the southeast Pacific coast demonstrates how local environmental factors, such as temperature and productivity, drive adaptive genetic differentiation (Figure 2). This differentiation is crucial for the species' ability to inhabit diverse ecological niches within the Humboldt Current System (Segovia et al., 2020).

Figure 2 Redundancy analysis (RDA) showing the relative contributions of oceanographic variables to the genetic structure of outlier and neutral genotypes. SNP genotypes in gray; individuals are represented by different colors according to their location according to the map in the right panel. Plot shows the most relevant variables obtained with ordistep and ordiR2step functions (Adopted from Segovia et al., 2020)

5 Case Study: Ascidians in Extreme Environments

5.1 Adaptation mechanisms in deep-sea Ascidians

Deep-sea environments present unique challenges such as high hydrostatic pressure, low temperatures, and limited light. While specific studies on deep-sea Ascidians are limited, insights can be drawn from related marine organisms. For instance, the genomic basis of adaptation in Arctic Charr (Salvelinus alpinus) to deep-water habitats has been explored, revealing significant genetic divergence between deep and shallow water morphs (Wang et al., 2024). Genes involved in processes such as gene expression, DNA repair, cardiac function, and membrane transport were identified as crucial for adaptation to deep-water conditions (Kess et al., 2021). These findings suggest that similar genomic mechanisms may be at play in deep-sea Ascidians, enabling them to thrive in such extreme environments.

5.2 Genomic responses to hypoxia in polar Ascidians

Polar regions are characterized by extreme cold and often hypoxic conditions. The leathery sea squirt, Styela clava, has shown significant genomic adaptations to cold environments, including the expansion of gene families related to heat-shock proteins and the horizontal transfer of cold-shock protein genes from bacteria (Wei et al., 2020). These adaptations likely play a crucial role in enabling Ascidians to survive in hypoxic polar waters. Additionally, studies on Ciona robusta and Ciona savignyi have demonstrated species-specific alternative splicing responses to environmental stresses, including temperature variations, which may also contribute to their ability to cope with hypoxic conditions (Figure 3) (Huang et al., 2023).

Figure 3 Gene expression and alternative splicing response of serine/arginine-rich splicing factor (SRSF) genes to environmental changes (Adopted from Huang et al., 2023)

5.3 Lessons from Ascidians in anthropogenic impacted areas (e.g., pollution)

Ascidians in areas impacted by human activities, such as pollution, exhibit notable genomic adaptations. For example, the Ascidian Pyura chilensis shows significant genetic differentiation across environmentally heterogeneous regions, driven by local adaptation to factors such as sea surface temperature and upwelling-associated variables (Segovia et al., 2020). Similarly, the marine invasive Ascidian Molgula manhattensis has demonstrated genomic signatures of local adaptation to salinity-related variables, highlighting the role of environmental selection in driving adaptive divergence (Chen et al., 2021). These studies underscore the importance of understanding the genomic basis of adaptation in Ascidians to predict their responses to anthropogenic changes and to develop effective conservation strategies.

6 Symbiotic Relationships and Their Genomic Impacts

6.1 Symbiosis with microorganisms in Ascidians

Ascidians, or sea squirts, are known to harbor diverse and host-specific microbial communities. These symbiotic relationships are crucial for the Ascidians' adaptation to various environments. For instance, studies have shown that Ascidians host a wide range of microbial symbionts, including bacteria and archaea, which are distinct from the surrounding seawater bacterioplankton. These microbial communities are involved in essential functions such as ammonia-oxidization, denitrification, and heavy-metal processing, which can enhance the host's tolerance to different environmental conditions (Evans et al., 2017). Additionally, the microbiomes of Ascidians have been found to include bacteria from phyla such as Cyanobacteria, Proteobacteria, Bacteroidetes, Actinobacteria, and Planctomycetes, which contribute to various ecological roles, including UV protection and defense against predators (Matos and Antunes, 2021).

6.2 Genomic modifications influenced by symbiotic interactions

Symbiotic interactions can lead to significant genomic modifications in both the host and the symbionts. For example, the genome of the Ascidian Styela clava has undergone expansion due to an increase in transposon numbers and variations in dominant types. This genomic expansion includes the horizontal transfer of cold-shock protein genes from bacteria, which likely aids in the adaptation to cold environments (Wei et al., 2020). Similarly, the genome of the sponge symbiont "Candidatus Synechococcus spongiarum" has undergone streamlining, losing genes related to environmental toxin resistance and polysaccharide biosynthesis, which suggests adaptation to the stable environment within the sponge host (Gao et al., 2014). These genomic changes highlight the dynamic nature of symbiotic relationships and their impact on the genetic architecture of the involved organisms.

6.3 Role of symbiosis in Ascidians' adaptation to extreme environments

Symbiotic relationships play a crucial role in the adaptation of Ascidians to extreme environments. The presence of specific microbial communities can enhance the host's ability to withstand harsh conditions. For instance, the microbial symbionts in Ascidians have been linked to functions such as heavy-metal processing and bioaccumulation, which can be vital for survival in polluted environments (Knobloch et al., 2019). Moreover, the integration of microbial genes into the host genome, such as the cold-shock protein genes in Styela clava, provides additional mechanisms for coping with extreme temperatures (Rúav et al., 2016). These symbiotic interactions not only facilitate the immediate survival of Ascidians in challenging environments but also drive long-term evolutionary adaptations through genomic modifications.

7 Environmental Stress and Adaptive Evolution in Ascidians

7.1 Impact of climate change on Ascidians

Climate change poses significant challenges to marine organisms, including Ascidians, by altering temperature and salinity levels in their habitats. The leathery sea squirt (Styela clava) has shown remarkable genomic adaptations to these changes, including the expansion of heat-shock protein genes and the horizontal transfer of cold-shock protein genes from bacteria, which help it survive in varied environmental conditions (Wei et al., 2020). Additionally, the estuarine oyster study highlights the role of gene expansion in solute carrier families, which are crucial for temperature and salinity stress responses, suggesting similar mechanisms might be at play in Ascidians (Li et al., 2021).

7.2 Evolutionary genomic responses to pollution and ocean acidification

Ascidians, like other marine organisms, face significant threats from pollution and ocean acidification. The study on the marine copepod Acartia tonsa provides insights into how marine species can adapt to multiple stressors, including warming and acidification, through polygenic responses targeting cellular homeostasis and stress response mechanisms (Brennan et al., 2021). Similarly, the rapid adaptation of killifish to polluted environments through introgression of toxicant-resistant genes from a related species underscores the potential for genetic variability to facilitate evolutionary rescue in Ascidians facing pollution (Oziolor et al., 2019). The genomic analysis of the invasive Ascidian Molgula manhattensis revealed significant genetic differentiation driven by local environmental factors, particularly salinity, indicating that pollution and other environmental stressors can drive adaptive divergence in Ascidian populations (Chen et al., 2021).

7.3 Molecular mechanisms underpinning resistance to environmental stressors

The molecular mechanisms that enable Ascidians to resist environmental stressors are diverse and complex. Proteomic studies on the stolon of Ciona robusta have identified key pathways involved in stress response, including cytoskeleton stability, signal transduction, and posttranslational modifications, which are crucial for maintaining structural integrity and activating stress responses under temperature and salinity stress (Li et al., 2021). Additionally, alternative splicing (AS) mechanisms play a significant role in the phenotypic plasticity of Ascidians, with species-specific and environmental context-dependent AS responses observed in Ciona robusta and Ciona savignyi, highlighting the importance of AS in rapid adaptation to environmental changes (Huang et al., 2023). The interplay between genetic and epigenetic variations also contributes to local adaptation, as seen in Ciona intestinalis populations, where DNA methylation patterns driven by local environments complement genetic adaptations, enhancing the rapid adaptive capacity of Ascidians (Chen et al., 2022).

Acknowledgments

I appreciate Dr H.Y. Wang for her assistance and thank the anonymous reviewers for their insightful comments and suggestions that improved the manuscript.

Conflict of Interest Disclosure

The author affirms that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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