Phageome

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Transmission electron micrograph of multiple bacteriophages attached to a bacterial cell wall Phage.jpg
Transmission electron micrograph of multiple bacteriophages attached to a bacterial cell wall

A phageome is a community of bacteriophages and their metagenomes localized in a particular environment, similar to a microbiome. [1] [2] Phageome is a subcategory of virome, which is all of the viruses that are associated with a host or environment. [3] The term was first used in an article by Modi et al. in 2013 [4] and has continued to be used in scientific articles that relate to bacteriophages and their metagenomes. A bacteriophage, or phage for short, is a virus that can infect bacteria and archaea, and can replicate inside of them. Phages make up the majority of most viromes and are currently understood as being the most abundant organism. [5] Oftentimes scientists will look only at a phageome instead of a virome while conducting research. Variations due to many factors have also been explored such as diet, age, and geography. The phageome has been studied in humans in connection with a wide range of disorders of the human body, including IBD, IBS, and colorectal cancer. [6]

Contents

In humans

Chart demonstrating variations in the phageome as seen due to age, disease, diet and methodological choices in research. Phage Variation.gif
Chart demonstrating variations in the phageome as seen due to age, disease, diet and methodological choices in research.

Although bacteriophages cannot infect human cells, they are found in abundance in the human virome. [7] Phageome research in humans has largely focused on the gut, however it is also being investigated in other areas like the skin, [8] blood, [9] and mouth. [10] The composition of phages that make up a healthy human gut phageome is currently debated, since different methods of research can lead to different results. [11] At birth, the human phageome, and the overall virome in general, is almost non-existent. [12] The human phageome is thought to be brought about in newborns through prophage induction of bacteria passed on from the mother vaginally during birth. [12] However, phages can be introduced through breastfeeding, made evident through studies finding near-exact matches of crAssphage sequences between mother and child. [12] Variations in the human gut phageome continue across the lifespan. Siphoviridae and Myoviridae are the most abundant in infants and their numbers wane into childhood, whereas Crassvirales dominate in adults. [13] The phageome can also experience changes as a result of diet, which can introduce new phages present in our foods. [6] For example, in those with gluten-free diets, crAssphage were noted in higher abundance along with decreases in the families of Podoviridae . [13] Global geographical differences in phageome composition have been noted, with further variation found within individuals living in rural and urban locations. [13] For instance, residents in Hong Kong, China were found to have less phages associated with targeting pathogenic bacteria in comparison to those in Yunnan province. [14] Furthermore, residing for longer periods of time in urban regions correlated with increases of Lactobacillus and Lactococcus phages. [14]

In disease

Changes in the phageome have been seen in various disorders affecting the human body. In the gut, unique changes in the phageome have been described in both inflammatory bowel disease and irritable bowel syndrome. [12] Even further specific changes exist in subtypes of the two disorders. IBS subtypes of IBS-D and IBS-C saw increases in different species belonging to Microviridae and Myoviridae. [12] In Ulcerative colitis and Crohn's disease, which are subtypes of IBD, differences in levels of Caudovirales richness and species have been found. [15] Furthermore, phages that target Acinetobacter have been found in the blood of patients with Crohn's disease. [9] This is thought to occur due to the compromised, inflamed gut barrier allowing for bacteriophage transfer. [9] In the mouth, periodontitis has been associated with Myoviridae residing under the gums along with a currently unspecified bacteriophage in the Siphoviridae family. [10] Phageome changes have also been described in metabolic disorders including type-1 diabetes, type-2 diabetes and metabolic syndrome. In type-1 diabetes, overall shifts have been seen in Myoviridae and Podoviridae. [6] The genome of bacteriophages residing in the gut in Type-2 diabetes patients have been shown to contain numerous genes implicated in disease development. [6] Total phage representation in the virome is higher in individuals with Cardiovascular disease than healthy controls, totaling 63% and 18% respectively. [6] Lastly, researchers studying Colorectal cancer have observed increased richness in a variety of phage genera, with the most notable differences seen in Inovirus and Tunalikevirus. [13]

See also

Related Research Articles

<span class="mw-page-title-main">Bacteriophage</span> Virus that infects prokaryotes

A bacteriophage, also known informally as a phage, is a virus that infects and replicates within bacteria and archaea. The term is derived from Ancient Greek φαγεῖν (phagein) 'to devour' and bacteria. Bacteriophages are composed of proteins that encapsulate a DNA or RNA genome, and may have structures that are either simple or elaborate. Their genomes may encode as few as four genes and as many as hundreds of genes. Phages replicate within the bacterium following the injection of their genome into its cytoplasm.

<span class="mw-page-title-main">Crohn's disease</span> Type of inflammatory bowel disease

Crohn's disease is a chronic inflammatory bowel disease characterized by recurrent episodes of intestinal inflammation, primarily manifesting as diarrhea and abdominal pain. Unlike ulcerative colitis, inflammation can occur anywhere in the gastrointestinal tract, though it most frequently affects the ileum and colon, involving all layers of the intestinal wall. Symptoms may be non-specific and progress gradually, often delaying diagnosis. About one-third of patients have colonic disease, another third have ileocolic disease, and the remaining third have isolated ileal disease. Systemic symptoms such as chronic fatigue, weight loss, and low-grade fevers are common. Organs such as the skin and joints can also be affected. Complications can include bowel obstructions, fistulas, nutrition problems, and an increased risk of intestinal cancers.

<span class="mw-page-title-main">Human microbiome</span> Microorganisms in or on human skin and biofluids

The human microbiome is the aggregate of all microbiota that reside on or within human tissues and biofluids along with the corresponding anatomical sites in which they reside, including the gastrointestinal tract, skin, mammary glands, seminal fluid, uterus, ovarian follicles, lung, saliva, oral mucosa, conjunctiva, and the biliary tract. Types of human microbiota include bacteria, archaea, fungi, protists, and viruses. Though micro-animals can also live on the human body, they are typically excluded from this definition. In the context of genomics, the term human microbiome is sometimes used to refer to the collective genomes of resident microorganisms; however, the term human metagenome has the same meaning.

<span class="mw-page-title-main">Irritable bowel syndrome</span> Functional gastrointestinal disorder

Irritable bowel syndrome (IBS) is a functional gastrointestinal disorder characterized by a group of symptoms that commonly include abdominal pain, abdominal bloating and changes in the consistency of bowel movements. These symptoms may occur over a long time, sometimes for years. IBS can negatively affect quality of life and may result in missed school or work or reduced productivity at work. Disorders such as anxiety, major depression, and chronic fatigue syndrome are common among people with IBS.

<span class="mw-page-title-main">Prophage</span> Bacteriophage genome that is integrated into a bacterial cell

A prophage is a bacteriophage genome that is integrated into the circular bacterial chromosome or exists as an extrachromosomal plasmid within the bacterial cell. Integration of prophages into the bacterial host is the characteristic step of the lysogenic cycle of temperate phages. Prophages remain latent in the genome through multiple cell divisions until activation by an external factor, such as UV light, leading to production of new phage particles that will lyse the cell and spread. As ubiquitous mobile genetic elements, prophages play important roles in bacterial genetics and evolution, such as in the acquisition of virulence factors.

<span class="mw-page-title-main">Inflammatory bowel disease</span> Medical condition

Inflammatory bowel disease (IBD) is a group of inflammatory conditions of the colon and small intestine, with Crohn's disease and ulcerative colitis (UC) being the principal types. Crohn's disease affects the small intestine and large intestine, as well as the mouth, esophagus, stomach and the anus, whereas UC primarily affects the colon and the rectum.

<i>Caudoviricetes</i> Class of viruses

Caudoviricetes is a class of viruses known as the tailed bacteriophages. Under the Baltimore classification scheme, the Caudoviricetes are group I viruses as they have double stranded DNA (dsDNA) genomes, which can be anywhere from 18,000 base pairs to 500,000 base pairs in length. The virus particles have a distinct shape; each virion has an icosahedral head that contains the viral genome, and is attached to a flexible tail by a connector protein. The order encompasses a wide range of viruses, many containing genes of similar nucleotide sequence and function. However, some tailed bacteriophage genomes can vary quite significantly in nucleotide sequence, even among the same genus. Due to their characteristic structure and possession of potentially homologous genes, it is believed these bacteriophages possess a common origin.

<span class="mw-page-title-main">Gut microbiota</span> Community of microorganisms in the gut

Gut microbiota, gut microbiome, or gut flora are the microorganisms, including bacteria, archaea, fungi, and viruses, that live in the digestive tracts of animals. The gastrointestinal metagenome is the aggregate of all the genomes of the gut microbiota. The gut is the main location of the human microbiome. The gut microbiota has broad impacts, including effects on colonization, resistance to pathogens, maintaining the intestinal epithelium, metabolizing dietary and pharmaceutical compounds, controlling immune function, and even behavior through the gut–brain axis.

A Bacillus phage is a member of a group of bacteriophages known to have bacteria in the genus Bacillus as host species. These bacteriophages have been found to belong to the families Myoviridae, Siphoviridae, Podoviridae, or Tectiviridae. The genus Bacillus includes the model organism, B. subtilis, and two widely known human pathogens, B. anthracis and B. cereus. Other strains of Bacillus bacteria that phage are known to infect include B. megaterium, B. mycoides, B. pseudomycoides, B. thuringiensis, and B. weihenstephanensis. More than 1,455 bacillus phage have been discovered from many different environments and areas around the world. Only 164 of these phages have been completely sequenced as of December 16, 2021.

Dysbiosis is characterized by a disruption to the microbiome resulting in an imbalance in the microbiota, changes in their functional composition and metabolic activities, or a shift in their local distribution. For example, a part of the human microbiota such as the skin flora, gut flora, or vaginal flora, can become deranged (unbalanced), when normally dominating species become underrepresented and species that normally are outcompeted or contained increase to fill the void. Similar to the human gut microbiome, diverse microbes colonize the plant rhizosphere, and dysbiosis in the rhizosphere, can negatively impact plant health. Dysbiosis is most commonly reported as a condition in the gastrointestinal tract or plant rhizosphere.

<span class="mw-page-title-main">Human Microbiome Project</span> Former research initiative

The Human Microbiome Project (HMP) was a United States National Institutes of Health (NIH) research initiative to improve understanding of the microbiota involved in human health and disease. Launched in 2007, the first phase (HMP1) focused on identifying and characterizing human microbiota. The second phase, known as the Integrative Human Microbiome Project (iHMP) launched in 2014 with the aim of generating resources to characterize the microbiome and elucidating the roles of microbes in health and disease states. The program received $170 million in funding by the NIH Common Fund from 2007 to 2016.

<i>Autographiviridae</i> Subfamily of viruses

Autographiviridae is a family of viruses in the order Caudovirales. Bacteria serve as natural hosts. There are 373 species in this family, assigned to 9 subfamilies and 133 genera.

Biological dark matter is an informal term for unclassified or poorly understood genetic material. This genetic material may refer to genetic material produced by unclassified microorganisms. By extension, biological dark matter may also refer to the un-isolated microorganisms whose existence can only be inferred from the genetic material that they produce. Some of the genetic material may not fall under the three existing domains of life: Bacteria, Archaea and Eukaryota; thus, it has been suggested that a possible fourth domain of life may yet be discovered, although other explanations are also probable. Alternatively, the genetic material may refer to non-coding DNA and non-coding RNA produced by known organisms.

<span class="mw-page-title-main">Human virome</span> Total collection of viruses in and on the human body

The human virome is the total collection of viruses in and on the human body. Viruses in the human body may infect both human cells and other microbes such as bacteria. Some viruses cause disease, while others may be asymptomatic. Certain viruses are also integrated into the human genome as proviruses or endogenous viral elements.

<span class="mw-page-title-main">Gut–brain axis</span> Biochemical signaling between the gastrointestinal tract and the central nervous system

The gut–brain axis is the two-way biochemical signaling that takes place between the gastrointestinal tract and the central nervous system (CNS). The term "microbiota–gut–brain axis" highlights the role of gut microbiota in these biochemical signaling. Broadly defined, the gut–brain axis includes the central nervous system, neuroendocrine system, neuroimmune systems, the hypothalamic–pituitary–adrenal axis, sympathetic and parasympathetic arms of the autonomic nervous system, the enteric nervous system, vagus nerve, and the gut microbiota.

<span class="mw-page-title-main">CrAssphage</span>

CrAss-like phage (crassviruses) are a bacteriophage family representing the most abundant viruses in the human gut, discovered in 2014 by cross assembling reads in human fecal metagenomes. In silico comparative genomics and taxonomic analysis have found that crAss-like phages represent a highly abundant and diverse family of viruses. CrAss-like phage were predicted to infect bacteria of the Bacteroidota phylum and the prediction was later confirmed when the first crAss-like phage (crAss001) was isolated on a Bacteroidota host in 2018. Crassviruses are podoviruses, possessing short non-contractile tails and icosahedral capsids. The first 3D structure of a crassvirus was determined by cryo-EM in 2023. While the presence of crAss-like phage in the human gut is not yet associated with any specific health condition, they are generally associated with a healthy gut microbiome and likely impact significantly on the gut Bacteroidota.

<span class="mw-page-title-main">Microbiome</span> Microbial community assemblage and activity

A microbiome is the community of microorganisms that can usually be found living together in any given habitat. It was defined more precisely in 1988 by Whipps et al. as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity". In 2020, an international panel of experts published the outcome of their discussions on the definition of the microbiome. They proposed a definition of the microbiome based on a revival of the "compact, clear, and comprehensive description of the term" as originally provided by Whipps et al., but supplemented with two explanatory paragraphs, the first pronouncing the dynamic character of the microbiome, and the second clearly separating the term microbiota from the term microbiome.

<span class="mw-page-title-main">Virome</span>

Virome refers to the assemblage of viruses that is often investigated and described by metagenomic sequencing of viral nucleic acids that are found associated with a particular ecosystem, organism or holobiont. The word is frequently used to describe environmental viral shotgun metagenomes. Viruses, including bacteriophages, are found in all environments, and studies of the virome have provided insights into nutrient cycling, development of immunity, and a major source of genes through lysogenic conversion. Also, the human virome has been characterized in nine organs of 31 Finnish individuals using qPCR and NGS methodologies.

<i>Bacteroides thetaiotaomicron</i> Species of bacterium

Bacteroides thetaiotaomicron is a Gram-negative, obligate anaerobic bacterium and a prominent member of the human gut microbiota, particularly within the large intestine. B. thetaiotaomicron belongs to the Bacteroides genus – a group that is known for its role in the complex microbial community of the gut microbiota. Its proteome, consisting of 4,779 members, includes a system for obtaining and breaking down dietary polysaccharides that would otherwise be difficult to digest for the human body.

Diversity-generating retroelements (DGRs) are a family of retroelements that were first found in Bordetella phage (BPP-1), and since been found in bacteria, Archaea, Archaean viruses, temperate phages, and lytic phages. DGRs benefit their host by mutating particular regions of specific target proteins, for instance, phage tail fiber in BPP-1, lipoprotein in legionella pneumophila, and TvpA in Treponema denticola . An error-prone reverse transcriptase is responsible for generating these hypervariable regions in target proteins. In mutagenic retrohoming, a mutagenized cDNA is reverse transcribed from a template region (TR), and is replaced with a segment similar to the template region called variable region (VR). Accessory variability determinant (Avd) protein is another component of DGRs, and its complex formation with the error-prone RT is of importance to mutagenic rehoming.

References

  1. ↑ Ma Y, You X, Mai G, Tokuyasu T, Liu C (February 2018). "A human gut phage catalog correlates the gut phageome with type 2 diabetes". Microbiome. 6 (1): 24. doi: 10.1186/s40168-018-0410-y . PMC   5796561 . PMID   29391057.
  2. ↑ Townsend EM, Kelly L, Muscatt G, Box JD, Hargraves N, Lilley D, et al. (4 June 2021). "The Human Gut Phageome: Origins and Roles in the Human Gut Microbiome". Frontiers in Cellular and Infection Microbiology. 11: 643214. doi: 10.3389/fcimb.2021.643214 . PMC   8213399 . PMID   34150671.
  3. ↑ Virgin HW (March 2014). "The virome in mammalian physiology and disease". Cell. 157 (1): 142–150. doi:10.1016/j.cell.2014.02.032. PMC   3977141 . PMID   24679532.
  4. ↑ Modi SR, Lee HH, Spina CS, Collins JJ (July 2013). "Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome". Nature. 499 (7457): 219–222. Bibcode:2013Natur.499..219M. doi:10.1038/nature12212. PMC   3710538 . PMID   23748443.
  5. ↑ Keen EC (January 2015). "A century of phage research: bacteriophages and the shaping of modern biology". BioEssays. 37 (1): 6–9. doi:10.1002/bies.201400152. PMC   4418462 . PMID   25521633.
  6. 1 2 3 4 5 Nabi-Afjadi M, Teymouri S, Monfared FN, Varnosfaderani SM, Halimi H (11 August 2023). "The Human Gut Phageome: Identification and Roles in the Diseases". Journal of Cellular Signaling. 4 (3): 128–141. doi:10.33696/Signaling.4.100. ISSN   2692-0638.
  7. ↑ Górska A, Peter S, Willmann M, Autenrieth I, Schlaberg R, Huson DH (June 2018). "Dynamics of the human gut phageome during antibiotic treatment". Computational Biology and Chemistry. 74: 420–427. doi:10.1016/j.compbiolchem.2018.03.011. PMID   29567068. S2CID   4222429.
  8. ↑ Wielscher M, Pfisterer K, Samardzic D, Balsini P, Bangert C, Jäger K, et al. (September 2023). "The phageome in normal and inflamed human skin". Science Advances. 9 (39): eadg4015. Bibcode:2023SciA....9G4015W. doi:10.1126/sciadv.adg4015. PMC   10541010 . PMID   37774017.
  9. 1 2 3 Lamy-Besnier Q, Theodorou I, Billaud M, Zhang H, Brot L, Culot A, et al. (19 September 2024), The human blood harbors a phageome which differs in Crohn's disease, doi:10.1101/2024.06.04.597176 , retrieved 2024-11-21
  10. 1 2 Szafrański SP, Slots J, Stiesch M (June 2021). "The human oral phageome". Periodontology 2000. 86 (1): 79–96. doi:10.1111/prd.12363. PMID   33690937.
  11. ↑ Shkoporov AN, Ryan FJ, Draper LA, Forde A, Stockdale SR, Daly KM, et al. (April 2018). "Reproducible protocols for metagenomic analysis of human faecal phageomes". Microbiome. 6 (1): 68. doi: 10.1186/s40168-018-0446-z . PMC   5892011 . PMID   29631623.
  12. 1 2 3 4 5 Zhang Y, Wang R (5 July 2023). "The human gut phageome: composition, development, and alterations in disease". Frontiers in Microbiology. 14: 1213625. doi: 10.3389/fmicb.2023.1213625 . PMID   37476672.
  13. 1 2 3 4 Tobin CA, Hill C, Shkoporov AN (15 September 2023). "Factors Affecting Variation of the Human Gut Phageome". Annual Review of Microbiology. 77: 363–379. doi:10.1146/annurev-micro-032421-105754. ISSN   1545-3251. PMID   37307857.
  14. 1 2 Zuo T, Sun Y, Wan Y, Yeoh YK, Zhang F, Cheung CP, et al. (11 November 2020). "Human-Gut-DNA Virome Variations across Geography, Ethnicity, and Urbanization". Cell Host & Microbe. 28 (5): 741–751.e4. doi:10.1016/j.chom.2020.08.005. ISSN   1934-6069. PMID   32910902.
  15. ↑ Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY, Keller BC, et al. (January 2015). "Disease-specific alterations in the enteric virome in inflammatory bowel disease". Cell. 160 (3): 447–460. doi:10.1016/j.cell.2015.01.002. PMID   25619688.
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