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What is the role of virome in human health? ​

Abstract ​

The human virome, a complex assembly of viruses residing within and on the human body, is increasingly recognized as a crucial player in health and disease. This intricate ecosystem encompasses a diverse range of viral entities, including bacteriophages and eukaryotic viruses, which dynamically interact with the host and other microbial communities. Recent advances in sequencing technologies and bioinformatics have illuminated the virome's potential significance in various physiological processes and disease mechanisms. Emerging evidence suggests that the virome can modulate immune responses, influence metabolic pathways, and contribute to the development of diseases such as autoimmune disorders, cancers, and chronic inflammatory conditions. The virome is believed to play a protective role against pathogenic bacteria, support metabolic functions, and aid in maintaining immune homeostasis. Furthermore, the early-life virome is particularly influential in establishing health trajectories, shaped by factors such as diet, environmental exposures, and host genetics. Understanding the virome's composition and dynamics offers promising avenues for diagnostic and therapeutic interventions, including phage therapy and microbiota modulation. Current research reveals the virome's dual role as both a beneficial and detrimental entity, highlighting the need for a nuanced understanding of how viral communities interact with host physiology. This review synthesizes current knowledge on the human virome, focusing on its composition, immune modulation, and implications for disease. It provides a comprehensive overview of the virome's role in human health, emphasizing the importance of considering viral communities within the broader context of microbiota research. By elucidating the complexities of the virome, this work aims to foster a deeper understanding of its impact on health and disease, ultimately guiding future research and therapeutic strategies.

Outline ​

This report will discuss the following questions.

  • 1 Introduction
  • 2 The Composition of the Human Virome
    • 2.1 Diversity of Viral Species
    • 2.2 Methods for Virome Characterization
  • 3 The Role of the Virome in Immune System Modulation
    • 3.1 Interactions with Host Immune Responses
    • 3.2 Influence on Autoimmunity and Inflammation
  • 4 The Virome and Human Diseases
    • 4.1 Viral Contributions to Cancer
    • 4.2 Virome in Metabolic Disorders
  • 5 Therapeutic Implications of the Virome
    • 5.1 Potential for Virome-based Therapies
    • 5.2 Future Directions in Virome Research
  • 6 Summary

1 Introduction ​

The human virome, an intricate assembly of viruses residing within and on the human body, is increasingly recognized as a crucial player in health and disease. This complex ecosystem encompasses a diverse range of viral entities, including bacteriophages and eukaryotic viruses, which interact dynamically with the host and other microbial communities. Unlike the extensively studied human microbiome, the virome has remained relatively underexplored until recent advances in sequencing technologies and bioinformatics have illuminated its potential significance in various physiological processes and disease mechanisms. Emerging evidence suggests that the virome can modulate immune responses, influence metabolic pathways, and even contribute to the development of diseases such as autoimmune disorders, cancers, and chronic inflammatory conditions [1][2].

The significance of the virome in human health cannot be overstated. It is believed to play a protective role against pathogenic bacteria, support metabolic functions, and aid in the maintenance of immune homeostasis [3][4]. Furthermore, the early-life virome is particularly influential in establishing health trajectories, with its composition shaped by factors such as diet, environmental exposures, and host genetics [5][6]. As such, understanding the virome's composition and dynamics offers promising avenues for diagnostic and therapeutic interventions, including phage therapy and microbiota modulation [1][7].

Current research on the virome reveals its dual role as both a beneficial and detrimental entity. On one hand, it is involved in enhancing immune responses and protecting against infections; on the other hand, dysregulation of the virome has been linked to various diseases, including inflammatory bowel disease, asthma, and even certain cancers [8][9]. This duality underscores the need for a nuanced understanding of how viral communities interact with host physiology and contribute to health and disease.

This review aims to synthesize current knowledge on the human virome, focusing on its composition, immune modulation, and implications for disease. The following sections will delve into the diversity of viral species present in the human body and the methodologies employed for virome characterization. We will explore the role of the virome in modulating immune system responses, particularly its interactions with host immunity and its influence on autoimmune and inflammatory conditions. Additionally, we will discuss the virome's contributions to various diseases, including its potential roles in cancer and metabolic disorders. Finally, we will examine the therapeutic implications of virome research, highlighting future directions and the potential for virome-based therapies.

In summary, this review will provide a comprehensive overview of the virome's role in human health, emphasizing the importance of considering viral communities within the broader context of microbiota research. By elucidating the complexities of the virome, we aim to foster a deeper understanding of its impact on health and disease, ultimately guiding future research and therapeutic strategies.

2 The Composition of the Human Virome ​

2.1 Diversity of Viral Species ​

The human virome is an intricate and dynamic component of the microbiome, encompassing a vast array of viral entities, including eukaryotic viruses, bacteriophages, and archaeal viruses. It plays a critical role in maintaining human health through its interactions with the host immune system and microbial communities.

The composition of the human virome is characterized by significant interindividual variability, influenced by factors such as age, diet, environment, and genetic predispositions. This virome is estimated to consist of approximately 10^13 viral particles per individual, which are primarily dominated by bacteriophages, particularly those from the order Crassvirales, commonly referred to as crAss-like phages. These phages contribute to the regulation of bacterial populations within the gut, thereby influencing microbial diversity and community structure [4].

The diversity of viral species within the virome is remarkable, with emerging evidence indicating that the viral community can adapt dynamically to environmental changes. For instance, metagenomic studies have revealed that the virome exhibits individual-specific patterns that evolve over time. This diversity is not merely a reflection of the presence of viruses but is crucial for the modulation of host immunity and metabolic processes [1]. Moreover, specific viral states within the virome have been associated with both health and disease outcomes. For example, certain viral populations may protect against diseases such as inflammatory bowel disease (IBD) and even some cancers, while dysbiosis of the virome has been linked to chronic inflammatory conditions and metabolic disorders [8].

In addition to shaping microbial community profiles, the virome is instrumental in modulating host immune responses. It interacts with immune cells, triggering various immune pathways that can either promote tolerance or activate inflammatory responses. Anelloviruses, for instance, are common components of the virome that persist in the human body without causing apparent disease, yet they may influence the immune system's response to other pathogens [10].

The role of the virome extends beyond the gut, impacting various organ systems and influencing overall health. Its interactions with other microbiome components and the host can lead to systemic effects, demonstrating that the virome is integral to maintaining homeostasis and preventing disease [6]. As research progresses, the potential of the virome as a diagnostic biomarker and therapeutic target is increasingly recognized, paving the way for innovative approaches in managing health and disease [2].

In summary, the human virome is a complex and essential element of the microbiome, contributing to health through its diverse viral species and dynamic interactions with the host and other microbiota. Its study not only enhances our understanding of microbial ecology but also opens new avenues for therapeutic interventions in various diseases.

2.2 Methods for Virome Characterization ​

The human virome, encompassing a vast array of viruses that inhabit the human body, plays a significant role in maintaining health and influencing disease processes. It is composed of various viral entities, including eukaryotic viruses, bacteriophages, and endogenous retroviruses. The virome interacts intricately with the human microbiome and the immune system, contributing to the regulation of immune responses and homeostasis.

The composition of the human virome is dynamic and highly individualized, with its establishment beginning at birth and continuing to evolve throughout life. The gut virome, in particular, is dominated by bacteriophages, which can modulate the bacterial communities within the gut, thereby impacting overall gut health and function. This composition is not static; it is influenced by factors such as diet, age, environmental exposures, and health status. Studies have shown that disruptions in the virome, such as those caused by infections or antibiotic use, can lead to dysbiosis, which is associated with various chronic diseases, including inflammatory bowel disease, metabolic disorders, and even neurodegenerative conditions[1][2][6].

Characterization of the virome has been significantly advanced by high-throughput sequencing technologies, particularly metagenomics. These methods allow for comprehensive profiling of viral communities, enabling researchers to identify both known and novel viral species. For instance, the use of shotgun sequencing has revealed the presence of diverse viral populations in various human ecological niches, such as the gastrointestinal tract and respiratory system[8][9][11]. Despite these advancements, a substantial portion of the virome remains uncharacterized, often referred to as "viral dark matter," which presents challenges in understanding its full impact on health and disease[4][8].

Moreover, the virome is increasingly recognized for its potential as a diagnostic biomarker and therapeutic target. For example, alterations in the virome have been linked to autoimmune diseases and cancers, suggesting that specific viral profiles may serve as indicators of disease risk or progression[2][8]. The ongoing exploration of the virome's role in human health underscores the need for standardized methodologies to improve our understanding of its complexities and to leverage this knowledge for clinical applications[2][9].

In summary, the human virome is a crucial component of the microbiome that influences health through its dynamic composition and interactions with the immune system. Advances in virome characterization methods are paving the way for a deeper understanding of its implications in health and disease, highlighting its potential for future therapeutic interventions.

3 The Role of the Virome in Immune System Modulation ​

3.1 Interactions with Host Immune Responses ​

The virome, which encompasses the collection of all viruses present in the human body, plays a crucial role in human health, particularly in the modulation of the immune system and its interactions with host immune responses. It includes both eukaryotic viruses and bacteriophages, contributing to the intricate balance of the microbiome.

One significant aspect of the virome's role is its interaction with the immune system. Viruses within the virome can trigger a broad range of immune responses, influencing both innate and adaptive immunity. For instance, the presence of certain viruses can activate inflammasomes, which are multiprotein complexes that play a critical role in the host's defense against pathogens. This activation can either enhance or dampen the immune response, depending on the context and the specific viral interactions involved [10].

Moreover, the virome is implicated in maintaining intestinal homeostasis and influencing systemic immune responses. The gut virome, in particular, is vital for shaping microbial community profiles and modulating host immunity. Studies have shown that perturbations in the gut virome are associated with chronic immune and inflammatory conditions, such as inflammatory bowel disease (IBD) and other autoimmune disorders [1][2]. The dynamic nature of the gut virome allows it to adapt to various environmental factors, including diet and lifestyle, which in turn affects the host's immune function and overall health [1].

The interactions between the virome and the immune system are complex and multifaceted. For example, viruses can modulate the activity of bacteria within the microbiome, which can further influence immune responses. This interplay suggests that the virome does not operate in isolation but is part of a larger network of microbial interactions that collectively shape the immune landscape of the host [12].

In addition to its direct effects on immune modulation, the virome may also serve as a potential biomarker for health and disease. Variations in the composition and diversity of the virome have been linked to various health outcomes, indicating that understanding these viral communities could lead to novel diagnostic and therapeutic approaches [8].

In summary, the virome is an integral component of human health, influencing immune system modulation through its interactions with host immune responses and other microbiome constituents. Its dynamic nature and ability to adapt to environmental changes highlight its potential role in maintaining health and contributing to disease pathogenesis. Understanding these interactions further emphasizes the importance of the virome in the broader context of human health and disease management.

3.2 Influence on Autoimmunity and Inflammation ​

The virome, comprising the diverse collection of viruses inhabiting the human body, plays a significant role in modulating immune responses and influencing various health conditions, particularly autoimmune diseases and inflammatory processes. Recent studies highlight the intricate interactions between the virome and the host immune system, suggesting that these viral entities can both promote and regulate immune responses.

Viruses within the virome, such as Anelloviruses, are typically present in most humans and persistently replicate without causing overt disease. These viruses have been shown to activate inflammasomes, which are multiprotein complexes that play a critical role in the innate immune response by sensing pathogens and orchestrating inflammation [10]. The modulation of immune responses by the virome can lead to either tolerance or activation of immune pathways, influencing how the host responds to various microorganisms [8].

The gut virome, in particular, has been implicated in shaping microbial community profiles and modulating host immunity. This interaction is crucial during early life, where the gut virome contributes to the establishment of immune pathways that influence lifelong health trajectories. Dysbiosis, or an imbalance in the virome, has been associated with chronic immune and inflammatory conditions, such as inflammatory bowel disease (IBD) and asthma [1], [8]. Specifically, alterations in the gut virome can lead to increased susceptibility to infections and chronic inflammation, thereby exacerbating autoimmune conditions [7].

Furthermore, the virome's role extends to influencing the pathogenesis of various diseases. For instance, in individuals with autoimmune disorders, the composition of the virome may reflect significant changes that correlate with disease severity and progression. The virome's interaction with the bacterial component of the microbiome is particularly noteworthy, as these interactions can either enhance or suppress immune responses, potentially leading to the development of autoimmune diseases [13].

In summary, the virome plays a crucial role in modulating immune system function, influencing inflammation, and potentially contributing to the development of autoimmune diseases. Its interactions with the host immune system and other microbiome components underscore its importance in maintaining health and preventing disease. Understanding these complex relationships further highlights the potential for therapeutic interventions targeting the virome to manage autoimmune and inflammatory conditions effectively.

4 The Virome and Human Diseases ​

4.1 Viral Contributions to Cancer ​

The human virome, comprising a vast array of viruses inhabiting the human body, plays a significant role in health and disease, particularly in the context of cancer. Understanding the virome's contributions involves exploring its composition, interactions with the microbiome, and potential mechanisms of disease modulation.

The human virome has gained prominence in recent years, particularly following the COVID-19 pandemic, due to its implications in various health conditions, including autoimmune diseases, inflammatory disorders, and cancers. The characterization of the human virome can be achieved through advanced techniques such as shotgun next-generation sequencing (metagenomics), which allows for the identification of viral communities within environmental samples and the discovery of previously uncharacterized viral families. Variations in viral quantity and diversity have been linked to disease development, primarily through their effects on gut bacterial microbiota [8].

In the gastrointestinal tract, the virome is essential for maintaining tissue homeostasis and health. It has been observed that disturbances in the virome can initiate or sustain oncogenic mechanisms, contributing to the onset of dysplastic processes and cancer progression. The interplay between the virome and the gut microbiota is particularly critical, as phages can regulate bacterial populations through mechanisms such as lysogeny, which may increase susceptibility to infections, chronic inflammation, and ultimately cancer [14].

Specific cancers, such as colorectal cancer, have been linked to alterations in the virome. Studies have shown that the virome associated with colorectal cancer is characterized by a predominance of temperate bacteriophages, which may influence cancer progression by altering the composition of bacterial communities in the gut [15]. This suggests that the virome may play an indirect role in cancer development by modulating the microbiota that interacts with the host's immune system.

Furthermore, the gut virome is implicated in chronic inflammatory conditions and metabolic disorders, which are risk factors for cancer. Research indicates that the early-life gut virome is particularly influential in shaping long-term health trajectories through its interactions with diet and immune pathways [1]. As such, the virome's dynamic nature and individual-specific patterns highlight its potential as a diagnostic biomarker and therapeutic target in cancer and other diseases [2].

In summary, the virome's role in human health, especially concerning cancer, is multifaceted. It not only contributes to the maintenance of microbial balance and immune regulation but also influences disease mechanisms through its interactions with other microbiome components. Understanding these relationships is crucial for developing novel therapeutic strategies and improving health outcomes in cancer patients and beyond.

4.2 Virome in Metabolic Disorders ​

The virome, a complex ecosystem of viruses residing within the human body, plays a significant role in various aspects of human health, particularly in relation to metabolic disorders. Recent studies have highlighted the intricate interactions between the virome and the gut microbiome, demonstrating that these viral entities can influence metabolic processes and contribute to the pathogenesis of several chronic diseases.

The gut virome is primarily composed of bacteriophages, which are viruses that infect bacteria. These bacteriophages are abundant in the gastrointestinal tract and can modulate bacterial populations through their lytic and lysogenic cycles. This modulation can impact the gut ecosystem and, consequently, metabolic pathways. For instance, alterations in the gut virome have been associated with metabolic disorders such as obesity, type 2 diabetes mellitus, and metabolic dysfunction-associated fatty liver disease [16].

Research has shown that changes in the gut virome can correlate with various metabolic conditions. For example, a study characterized the gut dsDNA virome in children with obesity and metabolic syndrome, revealing that phage richness and diversity increased in these individuals, which was associated with alterations in gut bacterial taxa and metabolic parameters [17]. This suggests that specific virome compositions may serve as biomarkers for metabolic health and disease.

Moreover, the gut virome has been implicated in the modulation of host immunity, which is crucial for maintaining metabolic health. The interactions between the virome and the immune system can influence inflammatory responses and metabolic regulation, further underscoring the virome's role in health and disease [1].

In the context of therapeutic applications, phage therapy is gaining renewed interest as a potential strategy to manipulate the gut virome and restore metabolic balance. Given the rise of antibiotic resistance, phage therapy offers a novel approach to precisely edit the gut microbiota, with promising applications in treating metabolic diseases [16].

Additionally, the virome's dynamic nature means that it can adapt to environmental factors, including diet, which further affects its role in health. Studies indicate that dietary intake can significantly influence the composition of the gut virome, which in turn may impact metabolic health [7].

In summary, the virome plays a multifaceted role in human health, particularly in metabolic disorders. It influences microbial community dynamics, modulates immune responses, and has potential therapeutic applications in restoring metabolic health. Continued research into the virome's interactions with other microbiome components and its implications for disease will be crucial for developing targeted interventions and understanding its contributions to human health.

5 Therapeutic Implications of the Virome ​

5.1 Potential for Virome-based Therapies ​

The human virome, comprising a diverse array of viruses inhabiting the human body, plays a crucial role in maintaining health and influencing disease processes. Recent studies have highlighted its therapeutic potential, particularly in the context of various diseases, including autoimmune disorders, inflammatory conditions, and cancers.

The gut virome is particularly significant, as it interacts dynamically with the gut microbiome and the host's immune system. It has been shown to modulate immune responses and maintain intestinal homeostasis. Disruptions in the virome have been associated with chronic diseases such as inflammatory bowel disease (IBD), Crohn's disease, and even metabolic disorders [1][2]. This underscores the virome's potential as a biomarker for disease and a target for therapeutic interventions.

Phage therapy, which utilizes bacteriophages to target pathogenic bacteria, represents a promising avenue for virome-based therapies. The gut virome's bacteriophages can regulate bacterial populations, thereby influencing health outcomes. This approach not only aims to restore microbial balance but also to enhance the host's immune defenses [8][18]. Additionally, phage therapy has shown potential in treating infections resistant to conventional antibiotics, thus addressing a significant public health challenge.

The virome's role extends beyond the gut, influencing respiratory health as well. The respiratory tract virome has been implicated in modulating immune responses to respiratory infections and chronic diseases such as asthma and chronic obstructive pulmonary disease (COPD). Research indicates that certain viral populations may act as modifiers of airway inflammation, potentially serving as therapeutic targets in respiratory conditions [6].

Moreover, the virome's involvement in cancer development has garnered attention. Variations in virome composition and diversity have been linked to oncogenic processes, particularly in the gastrointestinal tract. Understanding the interactions between the virome and host cells may reveal new therapeutic strategies for cancer treatment [8][14]. For instance, the modulation of the immune response by specific viral components could enhance the efficacy of existing cancer therapies.

In conclusion, the therapeutic implications of the virome are profound, with potential applications in phage therapy, cancer treatment, and management of chronic inflammatory diseases. Ongoing research into the virome's composition, dynamics, and interactions with the host will be critical in harnessing its therapeutic potential and developing virome-based interventions to improve human health. The integration of virome studies into clinical practice may pave the way for novel, microbiome-inspired therapies that address a range of health issues [19][20].

5.2 Future Directions in Virome Research ​

The human virome, comprising a diverse array of viruses inhabiting the human body, plays a crucial role in maintaining health and modulating disease processes. Recent studies have highlighted its significance in various physiological and pathological contexts, underscoring its potential as a therapeutic target and a diagnostic biomarker.

The virome contributes to immune system regulation, influencing both innate and adaptive immunity. It is increasingly recognized that viruses, including those that do not cause overt disease, can modulate immune responses and contribute to homeostasis. For instance, Anelloviruses, prevalent in most individuals, may activate inflammasomes, thereby impacting immune defenses and inflammation regulation [10]. Additionally, the gut virome interacts dynamically with gut bacteria, influencing microbial community structure and function, which is essential for metabolic processes and immune modulation [1].

Therapeutically, the virome presents promising avenues for intervention. Phage therapy, which utilizes bacteriophages to target pathogenic bacteria, is one such application that leverages the virome's natural capacity to influence bacterial populations [1]. Furthermore, understanding the virome's composition and dynamics could lead to the development of precision therapies aimed at restoring balance in the microbiome, particularly in conditions characterized by dysbiosis, such as inflammatory bowel disease (IBD) and other chronic inflammatory conditions [2].

Future directions in virome research should focus on several key areas. First, there is a need for standardized methodologies in virome analysis to overcome challenges related to genomic characterization and data interpretation [6]. Enhanced metagenomic sequencing techniques can facilitate the identification of novel viral taxa and their roles in health and disease. Second, longitudinal studies are essential to understand the temporal dynamics of the virome and its interactions with host factors, including diet, age, and genetic predisposition [1]. Finally, elucidating the causal relationships between specific virome components and disease outcomes will be crucial for translating virome research into clinical applications [19].

In summary, the virome is integral to human health, influencing immune responses and microbial interactions. Its therapeutic potential, particularly through phage therapy and microbiome modulation, warrants further exploration. As research progresses, understanding the virome's role in health and disease will likely lead to innovative strategies for disease prevention and treatment.

6 Conclusion ​

The human virome represents a critical and complex component of the microbiome, influencing various aspects of health and disease through its dynamic interactions with host immune responses and microbial communities. Key findings indicate that the virome not only contributes to immune modulation but also plays significant roles in the pathogenesis of diseases such as autoimmune disorders, cancers, and metabolic conditions. The diverse viral species within the virome exhibit substantial interindividual variability, shaped by factors such as age, diet, and environmental exposures. Current research highlights the dual nature of the virome, emphasizing its potential to be both beneficial and detrimental, depending on the context of its interactions. Future research should focus on refining virome characterization methodologies, exploring its temporal dynamics, and elucidating causal relationships between virome components and health outcomes. The potential for virome-based therapies, particularly in the context of phage therapy and microbiota modulation, underscores the importance of this field in developing innovative strategies for disease prevention and management.

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