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International Journal of Marine Science (online), 2024, Vol. 14 ISSN 1927-6648 http://aquapublisher.com/index.php/ijms © 2024 AquaPublisher, registered at the publishing platform that is operated by Sophia Publishing Group, foded in British Columbia of Canada. l Rights Reserved. Latest Content 2024, Vol. 14, No.5 【Review Article】 Genomic Basis of Environmental Adaptation in Ascidians 295-303 Lingfei Jin DOI: 10.5376/ijms.2024.14.0033 【Research Perspective】 Marine Biogeochemical Processes and Ecosystem Evolution: Observational and Predictive Approaches 304-311 Liting Wang, Haimei Wang DOI: 10.5376/ijms.2024.14.0034 【Research Insight】 Microbial Metabolism and Flux of Methane (CH4) in Marine Sediments and Water Columns 312-320 Ming Li, Congbiao You DOI: 10.5376/ijms.2024.14.0035 【Reaearch Report】 Optimizing Coral Farming: A Comparative Analysis of Nursery Designs for Acropora aspera, Acropora muricata, andMontipora digitata in Anantara Lagoon, Maldives 321-331 Migliaccio O. DOI: 10.5376/ijms.2024.14.0036 【Feature Review】 Zebrafish as a Model for Studying Ciliary Development and Disease 332-340 Fan Wang, Fei Zhao DOI: 10.5376/ijms.2024.14.0037
International Journal of Marine Science, 2024, Vol.14, No.5, 295-303 http://www.aquapublisher.com/index.php/ijms 295 Review Article Open Access Genomic Basis of Environmental Adaptation inAscidians Lingfei Jin Institute of Life Science, Jiyang College of Zhejiang A&F University, Zhuji, 311800, Zhejiang, China Corresponding email: lingfei.jin@jicat.org International Journal of Marine Science, 2024, Vol.14, No.5, doi: 10.5376/ijms.2024.14.0033 Received: 30 Jun., 2024 Accepted: 15 Aug., 2024 Published: 09 Sep., 2024 Copyright © 2024 Jin, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproductio4n in any medium, provided the original work is properly cited. Preferred citation for this article: Jin L.F., 2024, Genomic basis of environmental adaptation in Ascidians, International Journal of Marine Science, 14(5): 295-303 (doi: 10.5376/ijms.2024.14.0033) Abstract Ascidians is a type of invertebrate widely distributed in the ocean, adapted to various environmental niches and distributed from intertidal zones to extreme deep-sea environments. Studying the genomic adaptability of sea squirts is of great significance for understanding the survival strategies of marine invertebrates in complex environments. This study explores the genomic basis of adaptive evolution of sea squirts in different environments, including genomic features, molecular mechanisms related to environmental stress, genetic basis of habitat specialization, and the impact of symbiotic relationships on their genome. In addition, attention has been paid to the impact of environmental pressures such as climate change and pollution on the adaptive evolution of sea squirts, providing new insights into the evolution and adaptability research of marine invertebrates. Keywords Genomic adaptation; Ascidians; Environmental stress; Habitat specialization; Symbiotic relationships 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 ascidiangenomes 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 typeA(C. robusta), despite having a comparable number of genes. This expansion is attributed to an increase in
International Journal of Marine Science, 2024, Vol.14, No.5, 295-303 http://www.aquapublisher.com/index.php/ijms 296 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)
International Journal of Marine Science, 2024, Vol.14, No.5, 295-303 http://www.aquapublisher.com/index.php/ijms 297 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 HSPgene 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,
International Journal of Marine Science, 2024, Vol.14, No.5, 295-303 http://www.aquapublisher.com/index.php/ijms 298 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
International Journal of Marine Science, 2024, Vol.14, No.5, 295-303 http://www.aquapublisher.com/index.php/ijms 299 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) Image caption: (A) SRSF gene expression changes under recurrent high salinity stresses in C. robusta, of which Cr_SRSF7a and Cr_SRSF6b genes were excluded from differential expression analysis due to their low expression level. The Log2 foldchange values between treatment and control groups were used to draw the heatmap, and the color circles with black borders indicate significantly changed genes (adjusted p value < 0.05). (B) SRSFgene expression changes under low (LT) and high temperature (HT), and low (LS) and high salinity (HS) stresses in C. savignyi. (C) Transcript expression level of two isoforms of alternatively spliced gene (Cs_SRSF12) after 24 h of control and HT stress groups. (D) Percentage of two isoforms of Cs_SRSF12 gene. (E) Conserved domains of isoform1 (upper) and isoform2 (lower) (Adopted from Huang et al., 2023)
International Journal of Marine Science, 2024, Vol.14, No.5, 295-303 http://www.aquapublisher.com/index.php/ijms 300 5.3 Lessons fromAscidians 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 inAscidians 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 inAscidians' 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 inAscidians 7.1 Impact of climate change onAscidians 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).
International Journal of Marine Science, 2024, Vol.14, No.5, 295-303 http://www.aquapublisher.com/index.php/ijms 301 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 Ascidianpopulations (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. References Brennan R.S., deMayo J.A., Dam H.J., Finiguerra M., Baumann H., Buffalo V., and Pespeni M.H., 2021, Experimental evolution reveals the synergistic genomic mechanisms of adaptation to ocean warming and acidification in a marine copepod, Proceedings of the National Academy of Sciences, 119(38): e2201521119. https://doi.org/10.1073/pnas.2201521119 Cheaib M., Amirabad A.D., Nordström K.J.V., Schulz M.H., and Simon M., 2015, Epigenetic regulation of serotype expression antagonizes transcriptome dynamics in Paramecium tetraurelia, DNA Research, 22(4): 293-305. https://doi.org/10.1093/dnares/dsv014 Chen L., Fu C.M., and Wang G.Y., 2016, Microbial diversity associated with Ascidians: a review of research methods and application, Symbiosis, 71: 19-26. https://doi.org/10.1007/s13199-016-0398-7 Chen Y., Gao Y., Huang X., Li S., and Zhan A., 2021, Local environment‐driven adaptive evolution in a marine invasive ascidian (Molgula manhattensis), Ecology and Evolution, 11: 4252-4266. https://doi.org/10.1002/ece3.7322 Chen Y.Y., Ni P., Fu R.Y., Murphy K.J., Wyeth R.C., Bishop C.D., Huang X.H., Li S.G., and Zhan A.D., 2022, (Epi)genomic adaptation driven by fine geographical scale environmental heterogeneity after recent biological invasions, Ecological Applications, 34(1): e2772. https://doi.org/10.1002/eap.2772 Deng Z.C., Liu H., He C.K., Shou C.Y., and Han Z.Q., 2021, Heat shock protein 70 (HSP70) and heat shock transcription factor (Hsf) gene families in Cynoglossus semilaevis: genome-wide identification and correlation analysis in response to low salinity stress, Marine and Freshwater Research, 72(8): 1132-1141. https://doi.org/10.1071/MF20326 Evans J.S., Erwin P.M., Shenkar N., and López‐Legentil S.L., 2017, Introduced Ascidians harbor highly diverse and host-specific symbiotic microbial assemblages, Scientific Reports, 7(1): 11033. https://doi.org/10.1038/s41598-017-11441-4
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International Journal of Marine Science, 2024, Vol.14, No.5, 304-311 http://www.aquapublisher.com/index.php/ijms 304 Research Perspective Open Access Marine Biogeochemical Processes and Ecosystem Evolution: Observational and Predictive Approaches Liting Wang, Haimei Wang Hainan Institute of Biotechnology, Haikou, 570206, Hainan, China Corresponding author: haimei.wang@hibio.org International Journal of Marine Science, 2024, Vol.14, No.5, doi: 10.5376/ijms.2024.14.0034 Received: 15 Jul., 2024 Accepted: 30 Aug., 2024 Published: 17 Sep., 2024 Copyright © 2024 Wang and Wang, This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproductio4n in any medium, provided the original work is properly cited. Preferred citation for this article: Wang L.T., and Wang H.M., 2024, Marine biogeochemical processes and ecosystem evolution: observational and predictive approaches, International Journal of Marine Science, 14(5): 304-311 (doi: 10.5376/ijms.2024.14.0034) Abstract This study provides an overview of the importance of marine biogeochemical cycles and their impact on ecosystem evolution, explores major biogeochemical processes such as carbon, nitrogen, phosphorus, sulfur, and iron, and analyzes how these processes drive the long-term evolution of marine ecosystems. It also summarizes observational methods for studying marine biogeochemistry, including remote sensing, in situ measurement, and long-term observational networks, and discusses the application of climate models and ecosystem predictive models in describing the evolution of marine ecosystems, as well as the challenges encountered in modeling. The study emphasizes the development of observation and prediction methods to support long-term monitoring and scientific management of ecosystems. Keywords Marine biogeochemical processes; Carbon cycle; Ecosystem evolution; Remote sensing; Predictive models 1 Introduction Marine biogeochemical cycles are fundamental processes that govern the transformation and movement of bioessential elements such as carbon (C), nitrogen (N), and phosphorus (P) within marine ecosystems. These cycles are driven primarily by microorganisms through their metabolic activities, which include energy harvesting from light and inorganic chemical bonds for autotrophic carbon fixation. The interconnectedness of these cycles with energy fluxes across the biosphere is crucial for maintaining the structure and function of marine ecosystems (Dang and Chen, 2017; Grabowski et al., 2019). For instance, the marine nitrogen cycle involves multiple biogeochemical transformations mediated by microorganisms, which play a critical role in primary productivity and the uptake of atmospheric carbon dioxide (Pajares and Ramos, 2019). Similarly, the phosphorus cycle, which is tightly controlled by microbial processes, is essential for marine productivity and ecosystem structure (Duhamel et al., 2021). Understanding the evolution of marine ecosystems is vital for predicting how these systems will respond to environmental changes. Marine microorganisms, which drive biogeochemical cycles, are currently facing unprecedented anthropogenic changes, including shifts in seawater pH, temperature, and nutrient availability 7. These changes can have profound impacts on the biogeography, community structure, and adaptive evolution of marine microorganisms, ultimately affecting large-scale biogeochemical cycles (Hutchins and Fu, 2017). The role of redox-active compounds in aquatic systems highlights the importance of fluctuating redox conditions in maintaining high reactivity and influencing biogeochemical element cycles (Peiffer et al., 2021). The evolution of these processes over time is crucial for understanding the resilience and adaptability of marine ecosystems in the face of global change. This study comprehensively analyzes marine biogeochemical processes and ecosystem evolution through observation and prediction methods, exploring the coupling of carbon and energy fluxes in the marine environment, especially in the subtropical circulation of the North Pacific. It evaluates the application and limitations of biogeochemical models in different marine environments, further discusses the thermodynamic principles behind marine biogeochemical cycles and their impact on ecosystem modeling, in order to enhance our understanding of the mechanisms and predictions of marine biogeochemical cycles and their role in ecosystem evolution.
International Journal of Marine Science, 2024, Vol.14, No.5, 304-311 http://www.aquapublisher.com/index.php/ijms 305 2 Major Marine Biogeochemical Processes 2.1 Carbon cycle and oceanic carbon sequestration The carbon cycle in marine environments is a complex interplay of biological, chemical, and physical processes that regulate the movement and storage of carbon. One of the key components of this cycle is the sequestration of carbon in the ocean, which involves the uptake of atmospheric CO2 by marine organisms and its subsequent storage in various forms. The PISCES-v2 model, for instance, simulates the lower trophic levels of marine ecosystems and the biogeochemical cycles of carbon and other nutrients, providing insights into how carbon is cycled and stored in the ocean (Aumont et al., 2015; Zhang et al., 2024). The chemoattraction of marine fauna to dimethyl sulfide (DMS) plays a crucial role in natural iron fertilization, which in turn enhances carbon sequestration in high-nutrient, low-chlorophyll (HNLC) areas. This process highlights the interconnectedness of the carbon, iron, and sulfur cycles in marine ecosystems. 2.2 Nitrogen and phosphorus cycles The nitrogen and phosphorus cycles are fundamental to marine biogeochemistry, influencing primary productivity and ecosystem dynamics. Nitrogen cycling, driven by microbial processes, includes nitrogen fixation, nitrification, and denitrification. These processes are sensitive to environmental changes such as ocean acidification, which can alter the rates of nitrogen transformations and impact microbial community composition (Wannicke et al., 2018). The eco-energetic strategies of chemolithoautotrophic microorganisms, which participate in the nitrogen cycle, are essential for understanding how these processes respond to global change. Phosphorus, on the other hand, is a limiting nutrient in many marine environments. Recent advances have revealed a more dynamic and interconnected phosphorus cycle than previously understood, with significant implications for marine productivity and ecosystem structure. The coupling of phosphorus with carbon, nitrogen, and metal cycles underscores its integral role in marine biogeochemistry. 2.3 Sulfur and iron cycles Sulfur and iron cycles are closely linked with other biogeochemical processes in marine environments. Sulfur cycling, primarily driven by sulfate reduction, is a major component of the microbial ecology in marine sediments. This process is interconnected with the cycles of carbon, nitrogen, and iron, influencing both cellular and ecosystem-level processes (Wasmund et al., 2017). The role of sulfur-transforming microorganisms in these cycles is critical for understanding the overall biogeochemical dynamics of marine sediments. Iron, a limiting nutrient in many ocean regions, is recycled by marine biota, enhancing carbon assimilation and linking the iron and carbon cycles (Savoca, 2018). The interaction between sulfur, iron, and carbon cycles is further exemplified by the chemoattraction of marine fauna to DMS, which triggers iron recycling and augments carbon sequestration in HNLC waters. These interconnected cycles highlight the complexity and interdependence of marine biogeochemical processes. 3 Ecosystem Evolution in Response to Biogeochemical Changes 3.1 Long-term shifts in marine ecosystem structure Marine ecosystems are undergoing significant structural changes due to various biogeochemical alterations. Ocean acidification (OA) and warming are primary drivers of these shifts, leading to a simplification of ecosystem structure and function. This simplification is characterized by reduced energy flow among trophic levels and limited acclimation potential for many species (Gamfeldt et al., 2015). Habitat-forming species such as coralligenous reefs and Posidonia oceanica meadows are experiencing biomass reductions, which in turn affect the entire marine community and ecosystem services (Zunino et al., 2021). These changes suggest a reorganization of energy flows and a decrease in ecosystem size, indicating a high degree of ecosystem development but potentially suboptimal conditions from an anthropocentric perspective. 3.2 Impact of ocean acidification on ecosystem dynamics Ocean acidification is profoundly impacting marine ecosystems by altering the biogeochemical cycles and the structure of biogenic habitats. The decline in pH and carbonate saturation affects habitat-forming organisms, leading to decreased biodiversity in coral reefs and mussel beds, while potentially increasing it in seagrass and
International Journal of Marine Science, 2024, Vol.14, No.5, 304-311 http://www.aquapublisher.com/index.php/ijms 306 some macroalgal habitats. These habitat changes exacerbate the direct negative effects of OA on coastal biodiversity, although the predicted biodiversity increases in certain habitats are not always observed (Sunday et al., 2017; Wang, 2024). OA impacts nitrogen cycling processes, enhancing diazotrophic nitrogen fixation and reducing nitrification rates, which may shift the relative nitrogen pools and affect the upper water column's nutrient dynamics. 3.3 Changes in biodiversity and food webs 3.3.1 Shifts in marine predator-prey relationships The combined effects of ocean warming and acidification are altering predator-prey dynamics within marine ecosystems. Increased temperatures and CO2 levels affect primary production and metabolic rates, leading to mismatches between herbivores and carnivores. For instance, while temperature increases consumption and metabolic rates of herbivores, secondary production decreases with acidification, creating a mismatch with carnivores whose metabolic and foraging costs increase with temperature (Nagelkerken and Connell, 2015). These changes in predator-prey relationships can lead to shifts in community compositions, favoring non-calcifying species and microorganisms. 3.3.2 Adaptations of marine species to nutrient changes Marine species are adapting to nutrient changes driven by biogeochemical alterations such as ocean acidification. For example, the enhancement of diazotrophic nitrogen fixation under OA conditions suggests that certain nitrogen-fixing species may thrive, potentially altering microbial community compositions. However, the responses are species- and strain-specific, indicating that some species may be better adapted to these changes than others (Wannicke et al., 2018). The shifts from calcified to non-calcified habitats under OA conditions lead to decreased diversity of associated fish species, favoring those better adapted to simplified ecosystems dominated by algae (Cattano et al., 2020). These adaptations highlight the complex interplay between biogeochemical changes and marine species' responses, which ultimately shape ecosystem dynamics and biodiversity. 4 Observational Approaches to Studying Marine Biogeochemistry 4.1 Remote sensing and satellite observations Remote sensing and satellite observations have revolutionized the study of marine biogeochemistry by providing rapid and synoptic data across multiple spatial and temporal scales. These technologies are particularly useful for monitoring biodiversity in critical coastal zones, where human activities and climate change are causing rapid alterations (Figure 1) (Kavanaugh et al., 2021). Satellite-derived data, such as ocean color properties, allow for the observation of surface ocean biogeochemical processes with unprecedented coverage and resolution (Jönsson et al., 2023). However, challenges remain due to complex bio-optical signals and suboptimal algorithms, which can hinder accurate data retrieval. Recent advancements in remote sensing, such as the use of the Wasserstein distance, have improved the comparison of satellite data with model simulations, enhancing our understanding of temporal dynamics in the ocean (Hyun et al., 2021). This set of images presents a comprehensive study assessing the distribution, biomass, and environmental parameters of coastal ecosystems (such as kelp forests, coral reefs, and seagrass beds) using remote sensing and field observation techniques. It includes spectral reflectance data at different depths and the spatiotemporal variations of spatial distribution. Remote sensing and satellite observation technologies have greatly enhanced our ability to monitor and understand coastal ecosystems, especially in response to rapidly changing climate and human disturbances. Through these technologies, scientists can quickly and comprehensively obtain information on ecosystem health, providing a scientific basis and decision support for the conservation and management of coastal biodiversity. 4.2 In situ measurement technologies In situ measurement technologies are essential for obtaining high-resolution data on marine biogeochemical processes. Autonomous platforms, such as the Biogeochemical-Argo (BGC-Argo) floats, are equipped with sensors that measure key biogeochemical variables like oxygen, nitrate, pH, and chlorophyll a (Chai et al., 2020; Claustre et al., 2020). These platforms provide temporally and vertically resolved observations, filling large gaps
International Journal of Marine Science, 2024, Vol.14, No.5, 304-311 http://www.aquapublisher.com/index.php/ijms 307 in ocean-observing systems and supporting the management of ocean resources. Cost-effective in situ sensors have emerged, driven by advancements in miniaturization and mass production, enabling large-scale deployments and high-resolution data collection (Organelli et al., 2019). These technologies are crucial for understanding complex system processes and rapidly evolving changes in ocean biogeochemistry. Figure 1 Development of foundation species algorithms for moderate spectral resolution, higher spatial resolution sensors (Adopted from Kavanaugh et al., 2021) Image caption: (a) Mean macrocystis canopy biomass derived from Landsat satellite sensors. (b) Kelp persistence for San Miguel Island, California, using kelp canopy data derived from Landsat sensors. (c) Sentinel-2 composite image of the Florida Keys region where MBON surveys are regularly conducted. (d) Instrument used for in situ measurements of upwelling and downwelling irradiances above a patch reef during a field campaign in May 22, 2012, near Sugarloaf Key (red marker in c). (e) Reflectances over different depths above seagrasses. (f) Reflectances over different depths above patch reefs (Adopted from Kavanaugh et al., 2021) 4.3 Long-term observational networks Long-term observational networks are vital for monitoring changes in marine ecosystems and biogeochemical cycles over extended periods. The BGC-Argo project is building a global network of autonomous floats that provide continuous, high-quality data on biogeochemical properties. These networks support the evaluation of ongoing changes due to anthropogenic pressures, such as acidification and deoxygenation, and contribute to sustainable ocean management. Additionally, the European Marine Omics Biodiversity Observation Network (EMO BON) aims to establish standardized, coordinated, and long-term omics observation networks to assess biodiversity and ecosystem functioning on a large scale. Such networks enhance observational power and provide structured, comparable data, which are essential for effective conservation measures and sustainable use of marine resources (Santi et al., 2023). 5 Predictive Modeling of Marine Ecosystem Evolution 5.1 Climate models and ocean biogeochemistry Climate models play a crucial role in understanding and predicting the impacts of climate change on marine biogeochemical processes. These models integrate various environmental drivers such as ocean warming, acidification, and oxygen depletion to simulate the responses of marine ecosystems. For instance, process-based models have been developed to quantitatively integrate physiological and ecological processes, thereby advancing research and informing management strategies for marine fish populations (Koenigstein et al., 2016). Biogeochemical models are employed to simulate key ecosystem components like chlorophyll-a, nutrients, carbon, and oxygen cycles across different marine environments, although they still face limitations and assumptions that need addressing (Ismail and Al-Shehhi, 2023).
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