1 Introduction

Host-microbe interactions are fundamental to the health and well-being of all animals, including pets. These interactions encompass a complex and dynamic relationship between the host's immune system and the diverse microbial communities that inhabit various body sites. The microbiota, which includes bacteria, archaea, fungi, and viruses, plays a crucial role in the induction, education, and function of the host immune system (Belkaid and Harrison, 2017). This symbiotic relationship is maintained through intricate feedback loops and regulatory pathways that ensure immune tolerance to beneficial microbes while mounting protective responses against pathogens (Zheng et al., 2020). The skin, gut, and other mucosal surfaces are key sites where these interactions occur, influencing both local and systemic immune responses (Chen et al., 2018; Kogut et al., 2020).

The microbiota is essential for maintaining the health of pets, influencing various physiological processes such as digestion, metabolism, and immune function. In the gut, for example, the microbiota aids in nutrient absorption and helps regulate the host's metabolic processes (Wong et al., 2016). Moreover, the microbiota plays a pivotal role in the development and function of the immune system, contributing to the maintenance of mucosal homeostasis and protecting against pathogenic invasions (Morella and Koskella, 2017; Kogut et al., 2020). Disruptions in the microbiota-immune system balance can lead to immune-mediated diseases, including allergies, autoimmune disorders, and chronic inflammatory conditions (Ruff et al., 2020). Understanding these interactions is crucial for developing therapeutic strategies aimed at restoring and maintaining pet health.

This study explores the current understanding of how the microbiota influences immune development and function, the consequences of microbial imbalances, and the potential for microbiome-targeted therapies. By synthesizing findings from various studies, this study hopes to highlight the critical role of the microbiota in pet health and identify areas for future research.

2 The Microbiome in Pets

2.1 Composition and diversity of pet microbiomes

The microbiome in pets, much like in humans, consists of a diverse community of microorganisms that inhabit various parts of the body, including the gastrointestinal tract, skin, and oral cavity. These microbial communities play crucial roles in the health and disease states of their hosts. The composition and diversity of these microbiomes are influenced by a multitude of factors, including diet, environment, and host genetics. For instance, host genetic determinants have been shown to influence the gut microbiome composition across various animal species, including pets, by affecting the abundance of specific microbial taxa (Ryu and Davenport, 2022). Additionally, the interplay between the microbiome and the host's immune system is critical in maintaining homeostasis and preventing disease (Zheng et al., 2020).

2.2 Differences between pet species

The microbiomes of different pet species, such as dogs and cats, exhibit distinct compositions and diversities. These differences can be attributed to variations in diet, gut morphology, and host physiology. For example, dogs, being omnivores, have a different gut microbiome composition compared to cats, which are obligate carnivores. The specific dietary requirements and digestive processes of each species shape their respective microbiomes uniquely (Basic et al., 2022; Ryu and Davenport, 2022). Furthermore, the immune system's interaction with the microbiome also varies between species, influencing the stability and composition of these microbial communities (Zheng et al., 2020; Taylor and Vega, 2021).

2.3 Factors influencing microbiome composition

Several factors influence the composition and diversity of the microbiome in pets. Diet is a primary factor, with different types of food (e.g., commercial pet food, raw diets) leading to variations in microbial communities. Environmental factors, such as exposure to different microbiomes in the household or outdoor environments, also play a significant role (Bernardo-Cravo et al., 2020; Sarkar et al., 2020). Additionally, the use of antibiotics can disrupt the natural balance of the microbiome, leading to dysbiosis and potential health issues (Kupritz et al., 2021). Host genetics further modulate the microbiome by influencing immune responses and other physiological processes that affect microbial colonization and stability (Taylor and Vega, 2021; Ryu and Davenport, 2022).

Studies have shown that the abundance of the microbiome varies significantly between individuals, and both genetic and environmental factors jointly determine the extent of this variability (Figure 1a). Moreover, heritability calculations further reveal that certain microbes are highly correlated with the host genotype, as indicated by the strong correlation in microbial abundance between offspring and their parents (Figure 1b). Quantitative trait locus (QTL) mapping can be used to identify host genetic variations associated with microbial abundance, which is crucial for understanding how host genes influence the microbiome (Figure 1c) (Ryu and Davenport, 2022).

Figure 1 Methodology for studying genetic effects on the microbiome (Adopted from Ryu and Davenport, 2022) Image caption: (a) The abundances of individual taxa in the gut vary across individuals in a population (left). A major open question in microbiome research is to what extent environmental versus genetic factors determine the variability in microbial abundance in a population (right). (b) Heritability of a trait in animal studies is often calculated by comparing offspring trait values (microbial abundance) to the mid-parental traits (the average microbial abundance of the offspring's parents). Highly heritable microbes show a tighter correlation between offspring and mid-parental abundance measurements (left) compared to less-heritable microbes (right). (c) Quantitative trait locus (QTL) mapping identifies host genetic variation associated with microbial abundance. A significantly associated QTL is identified if bacterial abundance stratifies by genotype class (Adopted from Ryu and Davenport, 2022)

3 Host-Microbe Interactions and Immune System Dynamics

3.1 Mechanisms of microbial influence on the immune system

The interaction between host microbiota and the immune system is a complex and dynamic process that plays a crucial role in maintaining homeostasis and defending against pathogens. The gut microbiota, for instance, metabolizes proteins and complex carbohydrates, synthesizes vitamins, and produces numerous metabolic products that mediate cross-talk between gut epithelial and immune cells (Yoo et al., 2020). This interaction is essential for the development and function of both the innate and adaptive immune systems, as the microbiota helps train and develop major components of the host's immune system (Zheng et al., 2020). The immune system, in turn, orchestrates the maintenance of key features of host-microbe symbiosis, ensuring that the microbial load is tolerated but anatomically contained, while remaining reactive to microbial invasion (Kogut et al., 2020).

Host microbiota influence the immune system through metabolites, signaling molecules, and other mechanisms. These microbes not only provide essential nutrients to the host, such as short-chain fatty acids (SCFAs) and vitamins, but also help the host with defense and metabolic functions through their symbiotic relationships. For example, cellulose-fermenting bacteria in ruminants convert cellulose into metabolites that are accessible to the host, while commensal microbes in the human gut provide SCFAs, secondary bile acids, and essential vitamins (Figure 2). The symbiotic relationships between microbiota and hosts in different species, such as nitrogen-fixing Rhizobia in legume roots and bioluminescent bacteria in the bobtail squid, help to illustrate the central role of microbiota in the host's immune system (Popkes and Valenzano, 2020).

Figure 2 Host-specific microbiota (Adopted from Popkes and Valenzano, 2020) Image caption: Coevolution of microbes and multicellular hosts leads to mutualistic relationships. The host builds a dynamic ecological niche which provides nutrients and a stable environment to the microbes. The microbiota, in turn, provide nutrients and novel metabolic pathways. Clockwise, from top right: legume roots establish symbiotic interactions with Rhizobia bacteria in the soil, which fix nitrogen to molecular forms accessible to the plant. Species-specific microbiota in the hydra modulate spontaneous body contractions and prevent lethal fungal infections. In sap-feeding aphids, endosymbiotic Buchnera provide the host with essential amino acids lacking in the sap. Protists and flagellates in termites ferment lignocellulose from wood. The bobtail squid hosts symbiotic colonies of bioluminescent Aliivibrio fischeri in its light organ, helping with defence and hunting behaviours. In ruminants, cellulose-fermenting bacteria digest fibre-rich plants into host-accessible metabolites, such as short-chain fatty acids (SCFA). Commensal microbes in the human intestine provide nutrients like SCFA, secondary bile acids and essential vitamins. This figure was generated with Biorender (Adopted from Popkes and Valenzano, 2020)

3.2 Role of microbiota in immune development in young pets

The microbiota plays a pivotal role in the immune development of young pets, particularly during the perinatal period. The maternal and neonatal microbiome significantly influences immune cell ontogeny in the offspring during gestation and early postnatal life. This early-life interaction is crucial for regulating normal neurodevelopmental processes and establishing a robust immune system. The gut microbiota's influence on the immune system is not limited to the gastrointestinal tract but extends to peripheral lymphoid organs and the central nervous system, highlighting the systemic impact of these early microbial interactions (Pronovost and Hsiao, 2019).

3.3 Impact of dysbiosis on immune dysregulation and disease

Dysbiosis, or the negative alteration in microbial composition, can lead to significant immune dysregulation and contribute to various diseases. An impaired interaction between gut microbiota and the mucosal immune system can increase the abundance of potentially pathogenic bacteria, disrupt the epithelial barrier, and increase susceptibility to infections. Chronic dysbiosis is associated with inflammation, oxidative stress, and insulin resistance, which can lead to conditions such as type 2 diabetes, cardiovascular disease, inflammatory bowel disease, autoimmune diseases, and various cancers (Yoo et al., 2020). The disruption of the physiological balance between host and commensal microbes during ageing also leads to dysbiosis and associated disease states (Popkes and Valenzano, 2020).

3.4 Immune-mediated conditions linked to microbiota imbalance

The imbalance in host-microbiota interactions is linked to a rise in immune-mediated diseases, including autoimmune, allergic, and chronic inflammatory disorders. Modern environmental and lifestyle changes have drastically altered this evolutionarily ancient process, leading to breaches in immune tolerance and barriers. This promotes immune-mediated diseases by gut, oral, and skin microbiota (Ruff et al., 2020). Additionally, microbial dysbiosis has been consistently observed in patients with atopic dermatitis, food allergies, and asthma, with ongoing research investigating the molecular mechanisms linking changes in microbial populations with disease risk and endotypes (Forde et al., 2022). Understanding these mechanisms is crucial for developing therapeutic avenues that target the microbiota, barrier surfaces, or the host immune system to restore tolerance and homeostasis.

4 The Role of Probiotics and Prebiotics in Modulating Pet Microbiomes

4.1 Definition and mechanisms of action

Probiotics are live microorganisms that, when administered in adequate amounts, confer a health benefit on the host. Prebiotics, on the other hand, are non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one or a limited number of bacteria in the colon, thus improving host health. The mechanisms through which probiotics and prebiotics exert their effects include modulation of the gut microbiota composition, enhancement of the gut barrier function, and modulation of the host immune response (Liu et al., 2022; Mazziotta et al., 2023; Mousa et al., 2023).

Probiotics interact with the host's immune cells and commensal microflora to modulate specific immune functions and maintain immune homeostasis. They can stimulate intestinal immune cells and commensal microflora, leading to improved immune functions (Mazziotta et al., 2023). Prebiotics, by promoting the growth of beneficial bacteria, can lead to the production of short-chain fatty acids (SCFAs) that improve gut health and overall host physiology (Ashaolu, 2020).

4.2 Evidence from studies in pets

Several studies have demonstrated the beneficial effects of probiotics and prebiotics on the gut microbiota and immune system in pets. For instance, probiotics have been shown to modulate the gut microbiota composition, enhance the gut barrier function, and modulate the immune response in pets, similar to their effects in humans (Huang et al., 2022; Liu et al., 2022; Mousa et al., 2023). In pets, probiotics have been used to manage gastrointestinal disorders, improve immune responses, and even modulate allergic reactions. For example, studies have shown that probiotics can reduce the severity of allergic airway responses in pets, suggesting a role in managing respiratory allergies (Huang et al., 2022). Additionally, probiotics have been found to improve gut health by increasing mucus secretion and preventing the destruction of tight junction proteins, thereby reducing gut dysbiosis and intestinal leakage (Cristofori et al., 2021).

4.3 Clinical applications and future prospects

The clinical applications of probiotics and prebiotics in pets are vast and promising. They are currently used to manage gastrointestinal disorders, enhance immune responses, and modulate allergic reactions. The use of probiotics and prebiotics as dietary supplements in pets can provide health benefits similar to those observed in humans, such as improved gut health, enhanced immune function, and reduced inflammation (Huang et al., 2022; Liu et al., 2022; Mazziotta et al., 2023).

Future research should focus on understanding the specific strains of probiotics that are most beneficial for pets, the optimal dosages, and the long-term effects of their use. Additionally, the development of synbiotics, which combine probiotics and prebiotics, could offer synergistic benefits and further enhance the health of pets. The potential for probiotics and prebiotics to serve as adjunct therapies in managing chronic conditions such as non-alcoholic fatty liver disease (NAFLD) and other metabolic disorders in pets also warrants further investigation (Carpi et al., 2022).

5 Case Study: Microbiome-Based Interventions in Pets

5.1 Case study 1: probiotic therapy in canine atopic dermatitis

Canine atopic dermatitis (AD) is a prevalent inflammatory skin disease characterized by skin barrier dysfunction and cutaneous microbial dysbiosis. Recent studies have highlighted the potential of probiotics to modulate the gut microbiota and immune responses, which may have therapeutic implications for AD. Probiotics, particularly strains of Lactobacillus and Bifidobacterium, have been shown to influence the gut microbiota composition and enhance immune regulation in both humans and animals (Fang et al., 2019; Petersen et al., 2019; Fang et al., 2021).

In a study focusing on canine AD, it was found that the administration of specific probiotic strains could improve clinical symptoms and modulate the immune response. The study demonstrated that probiotics could increase the diversity of the gut microbiota, reduce the Firmicutes/Bacteroidetes ratio, and enhance the production of anti-inflammatory cytokines such as IL-10 (Fang et al., 2019; Santoro et al., 2023). These findings suggest that probiotic therapy could be a promising adjunctive treatment for managing canine AD by restoring microbial balance and improving immune function.

5.2 Case study 2: fecal microbiota transplant in cats with chronic diarrhea

Chronic diarrhea in cats is often associated with gut dysbiosis, where the balance of the intestinal microbiota is disrupted. Fecal microbiota transplant (FMT) has emerged as a potential therapeutic intervention to restore healthy gut microbiota and alleviate gastrointestinal symptoms. FMT involves the transfer of fecal material from a healthy donor to the gastrointestinal tract of the affected individual, aiming to re-establish a balanced microbial community (Garcia et al., 2019; Pilla and Suchodolski, 2020).

In a case study involving cats with chronic diarrhea, FMT was administered to evaluate its efficacy in resolving gastrointestinal symptoms. The results indicated significant improvements in stool consistency and frequency, as well as a reduction in gastrointestinal inflammation. The transplanted microbiota helped to re-establish a healthy microbial environment, which in turn supported the restoration of normal gut function (Pilla and Suchodolski, 2020). This case study underscores the potential of FMT as a viable treatment option for chronic gastrointestinal disorders in pets, highlighting the importance of a balanced gut microbiome for overall health.

5.3 Lessons learned and implications for clinical practice

The case studies on probiotic therapy in canine atopic dermatitis and fecal microbiota transplantation (FMT) in cats with chronic diarrhea provide valuable insights into the potential of microbiome-based interventions in veterinary medicine. Key lessons learned from these studies include the promise of microbiome modulation, where both probiotics and FMT have shown potential in modulating gut microbiota, which is crucial for maintaining immune homeostasis and overall health in pets (Garcia et al., 2019; Pilla and Suchodolski, 2020). Additionally, probiotic therapy has been found to enhance immune responses, particularly by increasing anti-inflammatory cytokines, which may help manage inflammatory conditions such as atopic dermatitis (Fang et al., 2019; Santoro et al., 2023). FMT, on the other hand, has demonstrated efficacy in restoring healthy gut microbiota and alleviating chronic gastrointestinal symptoms, highlighting the importance of microbial balance in gut health.

These findings have significant implications for clinical practice. Veterinarians should consider incorporating microbiome-based therapies as part of a comprehensive treatment plan for pets with conditions linked to microbial dysbiosis. Further research is needed to optimize these interventions, including identifying the most effective probiotic strains and refining FMT protocols. Ultimately, a better understanding of host-microbe interactions will pave the way for more targeted and effective treatments in veterinary medicine.

6 Comparative Analysis with Human Microbiome Studies

6.1 Similarities and differences in host-microbe interactions

Host-microbe interactions in pets and humans exhibit both striking similarities and notable differences. In both cases, the microbiome plays a crucial role in the development and function of the immune system, influencing both innate and adaptive immunity (Zheng et al., 2020). For instance, the gut microbiota in both humans and animals is involved in the regulation of immune responses and the maintenance of homeostasis (Morais et al., 2020). However, there are species-specific differences in microbiota composition and immune system responses that must be considered. For example, while the general mechanisms of microbial influence on host immunity are conserved, the specific microbial species and their interactions with the host can vary significantly between humans and pets (Basic et al., 2022).

6.2 Translational insights from human studies to veterinary medicine

Insights from human microbiome studies have significant translational potential for veterinary medicine. The use of microbial-based therapeutics in treating naturally occurring cancers in pets, for example, leverages knowledge gained from human studies on the immune system's interaction with microbes (Withers et al., 2019). Veterinary oncology can serve as a relevant translational model for human cancer therapy, as the natural progression of certain cancers in pets mirrors that in humans, providing a valuable platform for biomarker discovery and drug development (Pinard et al., 2022). Additionally, understanding the gut-brain axis in humans has opened new avenues for exploring similar interactions in pets, potentially leading to novel treatments for neurological disorders (Morais et al., 2020).

6.3 Ethical and practical considerations

When translating findings from human microbiome studies to veterinary medicine, several ethical and practical considerations must be addressed. Ethical concerns include ensuring the welfare of animals used in research and the potential risks associated with experimental treatments. Practically, differences in physiology, diet, and living environments between humans and pets can impact the applicability of human-derived data to veterinary contexts (Basic et al., 2022). Moreover, the use of pets in research must balance scientific objectives with the ethical obligation to minimize harm and distress to the animals (Kaganer et al., 2023). These considerations are crucial for the responsible advancement of microbiome research in veterinary medicine.

7 Future Directions in Research

7.1 Emerging technologies in microbiome research

The rapid advancement of next-generation sequencing (NGS) technologies has revolutionized microbiome research, enabling comprehensive analysis of microbial communities and their interactions with the host immune system. These technologies have facilitated the identification of microbial taxa and their functional roles, which are crucial for understanding host-microbe interactions in pets (Cullen et al., 2020). Additionally, the development of sophisticated bioinformatics tools and workflows has enhanced our ability to analyze metagenomic data, providing deeper insights into the composition and dynamics of the microbiome (Malla et al., 2019). Simple animal models, such as zebrafish and Drosophila melanogaster, have also emerged as valuable tools for microbiome research, offering cost-effective and time-efficient alternatives to mammalian models. These models help elucidate the mechanisms by which microorganisms influence host traits, including immune responsiveness and metabolic functions (Douglas, 2019).

7.2 Potential for personalized microbiome interventions in pets

The concept of personalized microbiome interventions holds significant promise for improving pet health. By tailoring microbiome-modulating therapies to the specific needs of individual pets, it may be possible to enhance their immune function and overall well-being. Recent studies have highlighted the potential of microbiome-targeted therapeutic interventions, such as probiotics and fecal microbiota transplants, in modulating host immunity and mitigating disease (Zheng et al., 2020). For instance, the use of naturally antipathogenic microbes has shown promise in preventing and treating infections by leveraging their unique metabolic properties (Cruz et al., 2022). Furthermore, understanding the dynamic interactions between the host, microbiome, and pathogens can inform the development of personalized vaccination strategies that optimize immune responses and disease outcomes (Kaganer et al., 2023).

7.3 Integrating microbiome research with veterinary practice

Integrating microbiome research into veterinary practice can significantly enhance the diagnosis, treatment, and prevention of diseases in pets. The microbiome's role in shaping host immunity and disease dynamics underscores the importance of incorporating microbiome analysis into routine veterinary care (Bernardo-Cravo et al., 2020). For example, understanding the social microbiome and its transmission within animal social networks can inform strategies to manage infectious diseases and improve herd health (Sarkar et al., 2020). Additionally, the application of microbiome research in veterinary practice can lead to the development of novel diagnostic techniques and interventional strategies, such as microbiome-based therapies and personalized nutrition plans (Cullen et al., 2020). By leveraging the insights gained from microbiome research, veterinarians can adopt a more holistic approach to pet health, ultimately improving the quality of care provided to their patients (Xue et al., 2020).

8 Concluding Remarks

The intricate interplay between host microbiota and the immune system is fundamental to both health and disease in pets. The microbiome significantly influences the development and function of the host's immune system, contributing to both innate and adaptive immunity. Beneficial symbiotic relationships between hosts and their microbiota have evolved to maintain homeostasis and protect against pathogens, while imbalances in these interactions can lead to immune-mediated disorders. Environmental factors also play a crucial role in shaping these dynamics, affecting disease outcomes through their impact on the microbiome. Additionally, specific microbial metabolites, such as bile acids, act as mediators in the bidirectional communication between the host and its microbiota, further influencing immune responses.

Understanding the host-microbiome interactions has profound implications for pet health and veterinary medicine. Recognizing the role of the microbiome in immune system development and disease can lead to more targeted therapeutic interventions. For instance, manipulating the microbiome through probiotics or dietary changes could help in managing or preventing immune-mediated diseases.

Moreover, considering environmental factors in disease management strategies can improve outcomes by addressing the external influences on the host-microbiome-pathogen dynamics. The potential of microbiome-targeted therapies, such as the use of bile acids to modulate immune responses, offers promising avenues for treating conditions like intestinal inflammation.

The field of host-microbe interactions in pets is rapidly evolving, with ongoing research shedding light on the complex mechanisms underlying these relationships. Future studies should aim to achieve a more causal understanding of how specific microbial communities and their metabolites influence immune responses and disease outcomes. Additionally, exploring the impact of various environmental factors on the microbiome and immune system will be crucial in developing comprehensive disease management strategies. As our knowledge expands, the integration of microbiome science into veterinary practice holds the potential to revolutionize pet healthcare, leading to more personalized and effective treatments. Continued research and collaboration across disciplines will be essential in harnessing the full potential of microbiome-targeted therapies for improving pet health and well-being.

Acknowledgments

AnimalSci Publisher extends sincere thanks to two anonymous peer reviewers for their feedback on 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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