Comprehensive transcriptomics and proteomics analysis of Carassius auratus gills in response to Aeromonas hydrophila

Hu, Xiucai; Bai, Jie; Liu, Rongrong; Lv, Aijun

doi:10.1016/j.fsirep.2022.100077

Cited by 7 publications

(4 citation statements)

References 60 publications

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“…This indicates that both the gills and liver work in synergy to mitigate potential cellular damage from oxidative stress and maintain cellular redox balance. However, given that gills are one of the major surface tissues continuously exposed to the external environment, and also serve as a first line of defense against potential infections (Harper & Wolf, 2009; Hu et al, 2023), selective activation of immune responses in this tissue alone could be a preventive measure against opportunistic infections under CO 2 stress as has been previously observed under elevated CO 2 conditions (De Souza et al, 2014; Machado et al, 2020). Similar differences in tissue-specific regulation of specific metabolic pathways were observed between the gills and liver in all elevated CO 2 treatments.…”

Section: Discussionmentioning

confidence: 95%

“…Interestingly, genes involved in immune response were upregulated in the gills but downregulated in the liver indicating tissue-specific regulation of this function. Gills are one of the major surface tissues, which are continuously exposed to the external environment, and also serve as a first line of defense against potential infections (Harper & Wolf, 2009; Hu et al, 2023). Activation of immune responses has been previously observed under elevated CO 2 conditions which could be a preventive measure against opportunistic infections under CO 2 stress (De Souza et al, 2014; Machado et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

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Cross-talk between tissues is critical for intergenerational acclimation to environmental change

Suresh,

Welch,

Munday

et al. 2023

Preprint

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An organism’s reaction to environmental changes is mediated by coordinated responses of multiple tissues. Additionally, parental priming may increase offsprings’ acclimation potential to changing environmental conditions. As acidification of oceans continues to intensify it is critical to assess the acclimation potential of species at the whole organismal scale. To do this we need to understand the cross-talk between tissues in regulating and responding to pH changes. Here by using a multi-tissue approach we determine the influence of 1) variation in parental behavioural tolerance and 2) parental environment, on molecular responses of their offspring in a coral reef fish. The gills and liver showed the highest transcriptional response to OA conditions in juvenile fish regardless of the parental environment, while the brain and liver showed the greatest signal of intergenerational acclimation. Key functional pathways that were altered in the brain and liver upon within-generational CO2exposure were restored to control levels when parents were exposure to OA conditions. Furthermore, the expression of a new complement of genes involved in key functions were altered in the offspring only when the parents were previously exposed to OA conditions. Therefore, previous parental conditioning to ocean acidification can reprogram tissue transcriptomic profiles of the offspring enabling them to better cope in an environment with elevated CO2levels. Overall, our results show that intergenerational plasticity is key in evolutionarily adaptation to global change and illustrates how transcriptional changes across multiple tissues integrate to facilitate organismal acclimation to OA.Significance statementWith the global climate changing rapidly, organisms need to acclimate to the new conditions to survive. Assessing the adaptive potential of complex organisms such as vertebrates is especially challenging as each tissue has its own unique function. However, acclimation of organisms to changes in their environment requires functional integration of all tissues which is usually overlooked in climate change research. Here we reveal that cross-communication between tissues is crucial in the adaptive response of organisms to future ocean conditions. Furthermore, both parental environment and parental behavioral variability influence the transcriptional reprograming of offspring tissues in response to elevated CO2. Overall, it is the integration of transcriptional changes across multiple tissues that mediates intergenerational plasticity to future changes in ocean chemistry.

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Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Cross-talk between tissues is critical for intergenerational acclimation to environmental change

Suresh,

Welch,

Munday

et al. 2023

Preprint

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“…The study by Hu et al, delve through transcriptomics and proteomics to identify mucosal immunity i.e. first line of defence in gills of Carassius auratus against Ah (12). With the tangent of liver tissue analysis, a proteomic study suggests that Ah infection modulates host metabolic pathways and innate immunity with identified markers such as Toll like receptors and C-lectins in Labeo rohita (13).…”

Section: Introductionmentioning

confidence: 99%

Proteomic analysis of gut inLabeo rohitareveals ECM as Key Player in host’s Response toAeromonas hydrophilaInfection

Nissa,

Pinto,

Ghosh

et al. 2024

Preprint

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In the aquaculture sector, one of the challenges include disease outbreaks such as bacterial infections, particularly fromAeromonas hydrophila(Ah), impacting both wild and farmed fish. In this study, we conducted a proteomic analysis of the gut tissue inLabeo rohitafollowingAhinfection to elucidate the protein alterations and its implications for immune response. Our findings reveal significant dysregulation in extracellular matrix (ECM) associated proteins duringAhinfection, with increased abundance of elastin and Collagen alpha-3(VI) contributing to matrix rigidity. Pathway and enrichment analysis of differentially expressed proteins (DEPs) highlights the involvement of ECM-related pathways, including Focal adhesions, Integrin cell surface interactions, and actin cytoskeleton organization.Focal adhesions, crucial for connecting intracellular actin bundles to the ECM, play a pivotal role in immune response during infections. Increased abundance of integrin alpha 1, integrin beta 1, and Tetraspanin suggests their involvement in the host’s response toAhinfection. Proteins associated with actin cytoskeleton reorganization, such as myosin, tropomyosin, and phosphoglucomutase, exhibit increased abundance, influencing changes in cell behavior. Additionally, upregulated proteins like LTBP1 and Fibrillin-2 contribute to TGF-β signaling and focal adhesion, indicating their role in immune regulation.The study also identifies elevated levels of laminin, galectin 3, and tenascin-C, which interact with integrins and other ECM components, influencing immune cell migration and function. These proteins, along with decorin and lumican, act as immunomodulators, coordinating pro- and anti-inflammatory responses. ECM fragments released during pathogen invasion serve as “danger signals,” initiating pathogen clearance and tissue repair through Toll-like receptor signaling.IMPORTANCEThe study underscores the critical role of the extracellular matrix (ECM) and its associated proteins in the immune response of aquatic organisms during bacterial infections likeAeromonas hydrophila(Ah). Understanding the intricate interplay between ECM alterations and immune response pathways provides crucial insights for developing effective disease control strategies in aquaculture. By identifying key proteins and pathways involved in host defense mechanisms, this research lays the groundwork for targeted interventions to mitigate the impact of bacterial infections on fish health and aquaculture production.

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“…In recent years, an increasing number of studies have endeavored to utilize multi-omics data to elucidate the underlying factors contributing to gill tissue toxicity. Transcriptomic and proteomic analyses have demonstrated the immune deficiencies in the gill of crucian carp in response to Aeromonas hydrophila [ 37 ]. The utilization of transcriptomics and metabolomics methodologies unveiled the gill toxicity of crucian carp induced by DEHP [ 21 ].…”

Section: Introductionmentioning

confidence: 99%

Conventional Anthelmintic Concentration of Deltamethrin Immersion Disorder in the Gill Immune Responses of Crucian Carp

Wu,

Yuan,

Gao

et al. 2023

Toxics

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Current treatment strategies for parasitic infectious diseases in crucian carp primarily rely on chemotherapy. As a commonly used antiparasitic agent, deltamethrin (DEL) may have the potential adverse effects on external mucosa of fish such as gills. In this study, 180 healthy juvenile crucian carp (Carassius auratus) (average weight: 8.8 ± 1.0 g) were randomly divided into three groups for 28 days, which were immersed in 0 μg/L, 0.3 μg/L, and 0.6 μg/L of DEL, respectively. The results of histological analysis revealed that severe hyperplasia in the secondary lamellae of gills was observed, and the number of goblet (mucus-secreting) cells increased significantly after DEL immersion. TUNEL staining indicated that the number of apoptotic cells increased in crucian carp gill. At the molecular level, the mRNA expression analysis revealed significant upregulation of apoptosis (caspase 3, caspase 8, and bax), autophagy (atg5 and beclin-1), and immune response (lzm, muc5, il-6, il-8, il-10, tnfα, ifnγ, tgfβ, tlr4, myd88, and nf-kb), whereas tight junction-related genes (occludin and claudin12) were downregulated after DEL immersion, suggesting that DEL immersion altered innate immunity responses and promoted mucus secretion. Moreover, tandem mass tag (TMT)-based proteomics revealed that a total of 428 differentially expressed proteins (DEPs) contained 341 upregulated DEPs and 87 downregulated DEPs with function annotation were identified between the control and DEL groups. Functional analyses revealed that the DEPs were enriched in apoptotic process, phagosome, and lysosome pathways. Additionally, DEL immersion also drove gill microbiota to dysbiosis and an increase in potentially harmful bacteria such as Flavobacterium. Overall, this study showed that DEL elicited shifts in the immune response and changes in the surface microbiota of fish. These results provide new perspectives on the conventional anthelmintic concentration of DEL immersion disorder of the gill immune microenvironment in crucian carp and theoretical support for future optimization of their practical application.

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Comprehensive transcriptomics and proteomics analysis of Carassius auratus gills in response to Aeromonas hydrophila

Cited by 7 publications

References 60 publications

Cross-talk between tissues is critical for intergenerational acclimation to environmental change

Cross-talk between tissues is critical for intergenerational acclimation to environmental change

Proteomic analysis of gut inLabeo rohitareveals ECM as Key Player in host’s Response toAeromonas hydrophilaInfection

Conventional Anthelmintic Concentration of Deltamethrin Immersion Disorder in the Gill Immune Responses of Crucian Carp

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