CrAssphage

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crAss-like phage (crassvirus)
PhicrAss001.webp
3D structure of the ΦcrAss001 virus particle. a, Molecular surface of the viral particle (virion), viewed from the outside. b, Cross-section through the virion. Proteins making up the capsid (protein shell) are shown in yellow and blue; cargo proteins are in purple; pink and pale-blue proteins on the capsid are head-fibre proteins; proteins making up the tail barrel are shown in different colours; and tail-fibre proteins are shown in grey. Credit: Bayfield, O. W. et al./Nature (CC BY 4.0).
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Duplodnaviria
Kingdom: Heunggongvirae
Phylum: Uroviricota
Class: Caudoviricetes
Order:Crassvirales
Families

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. [1] In silico comparative genomics and taxonomic analysis have found that crAss-like phages represent a highly abundant and diverse family of viruses. [2] [3] 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 ( Bacteroides intestinalis) in 2018. [4] 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. [5] [6] 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 . [3] [2] [7] [8]

Contents

Discovery

The crAss (cross-assembly) software used to discover the first crAss-like phage, p-crAssphage (prototypical-crAssphage), relies on cross assembling reads from multiple metagenomes obtained from the same environment. [9] The goal of cross-assembly is that unknown reads from one metagenome align with known reads, or reads that have similarity to known reads, in another metagenome, thereby increasing the total number of usable reads in each metagenome. The crAss software is an analysis tool for cross-assemblies which specializes in reference-independent comparative metagenomics. [9] CrAss assumes that a contig(s) made up of reads from differing metagenomes (cross-contig) is representative of a biological entity present in each of the differing metagenomes. [9] P-crAssphage was discovered when crAss was used to analyze the cross-assembly of twelve human fecal metagenomes. Several cross-contigs consisting of unknown reads were identified in all twelve individuals and through re-assembly techniques, the p-crAssphage genome was re-constructed. [1] P-crAssphage has a ~97kbp circular DNA genome which contains 80 predicted open reading frames. Using co-occurrence analysis and CRISPR spacer similarities, the phage was predicted to infect Bacteroidota bacteria [1] which are dominant members of the gut microbiome in most individuals. [10]

Taxonomy

The crAss-like phage bacteriophage family is considered highly diverse and consists of four subfamilies- alpha, beta, delta, and gamma- and ten genera within the subfamilies. The subfamilies are defined by crAss-like phage that share 20–40% of their protein-encoding genes while a genera is characterized by crAss-like phage that share >40% of protein-encoding genes. The alpha subfamily consists of the greatest number of crAss-like phage representatives, including p-crAssphage. [11]

Morphology

Crassviruses are podoviruses, possessing short non-contractile tails and icosahedral capsids. [5] [4]

Replication

Based on initial sequence-based studies of crAss-like phage, the bacteriophage family was predicted to consist of phage with a diversity of lifestyles including lytic, lysogenic, and temperate. [12] [3] Despite the genetic evidence of certain lifestyles, in vitro studies of crAss-like phage replication strategies have yielded inconclusive results.

crAss001 and B. intestinalis

CrAss001 and its host, B. intestinalis, demonstrate a unique relationship in which the host and phage are able to stably co-exist and co-replicate in liquid culture, yet the phage efficiently lysis its host on solid agar substrates. [4] Co-existence of a phage and its host would typically be indicative of a lysogenic lifestyle, but the crAss001 genome contains none of the genes needed for lysogeny. It was hypothesized that crAss001 uses a lesser-known replication strategy like pseudolysogeny or a carrier state, [4] but a recent study has found evidence that the host is at least partially responsible for the stable co-existence through phase variation. [13] It's now thought that B. intestinalis can modulate infection of crAss001 by modifying its capsular polysaccharides (an example of phase variation), some of which the phage uses for host-recognition. With phase variation, B. intestinalis can maintain subpopulations both resistant and susceptible to phage infection, thereby generating a unique environment in which crAss001 has consistent access to hosts (susceptible subpopulation) and B. intestinalis can replicate uninhibited by phage (resistant subpopulation). [13] CrAss001 is still thought to infect the susceptible subpopulation using a pseudolysogenic or carrier state infection approach, both of which can be associated with a slow-release of phage from living bacterial hosts. The combination of host phase-variation and phage infection strategy yield a relationship in which the phage and host can exist in a stable equilibrium. [13]

crAss002 and B. xylanisolvens

CrAss002 also exhibits an unusual relationship with its host, B. xylanisolvens. [14] When crAss002 is inoculated into a culture of B. xylanisolvens, the phage takes several days of co-culturing to begin propagating after which it maintains a stable and relatively high titer. When isolated colonies of the co-cultured B. xylanisolvens were used to start new phage propagations, the colonies demonstrated varying responses to phage infection. Some cultures immediately supported phage propagation while others took several days. [14] The differing responses of B. xylanisolvens indicated that the bacterial population was mixed and consisted of cells both susceptible and resistant to phage infection, similar to the subpopulations of susceptible and resistant hosts in the crAss001 and B. intestinalis phage-host relationship. Similar to crAss001, crAss002 does not possess the genes needed for lysogeny. [14]

crAss001 and crAss002 in a bacterial community

In an attempt to see how crAss-like phage behaved in bacterial communities, crAss001 and crAss002 were inoculated into bioreactors containing a defined bacterial community representative of the human gut microbiota. The bacterial community included B. intestinalis and B. xylanisolvens, the respective hosts of crAss001 and crAss002. Despite the crAss001 and crAss002 titers increasing after infection, the cell counts of the bacterial community members were seemingly unaffected by the phage presence. [14] The phage and bacterial community maintained stable population levels throughout the experiment, mimicking the behavior of crAss001 and crAss002 in pure-cultures. It's hypothesized that crAss-like phage and their hosts use unique mechanisms or combinations of mechanisms to maintain their stable equilibrium. [14]

Humans and crAss-like phage

CrAss-like phage have been identified as a highly abundant and near-universal member of the human gut microbiome. [1] [11] CrAss-like phage seem to be more prevalent in those that consume a western diet which favors the phages' host bacterial phylum, Bacteroidota. [15] An evolutionary study of crAss-like phage and humans suggests that crAss-like phage prevalence amongst human populations expanded during industrialization and subsequent urbanization when a western diet become more common than a traditional hunter-gatherer diet. [15] Another study, however, found evidence that the relationship between crAss-like phage and humans may extend back to the evolution of the human origin. [8]

Due to the abundance and ubiquity of crAss-like phage in human populations, crAss-like phage have been tested as a method for detecting human feces. The virus may outperform indicator bacteria as a marker for human fecal contamination. [16] [17] [18] [19]

crAssphage RNA polymerase 248997 web crAssphage-RNA-Polymerase.jpg
crAssphage RNA polymerase

The presence of crAss-like phage in human gut microbiomes has not yet been associated with variables relating to lifestyle or health and it is widely considered that crAss-like phage are benign inhabitants of many people's gut microbiome. [3] [11] [15] [20] While the presence of crAss-like phage does not seem to be a good indicator of health status, it is possible that the absence of crAss-like phage from the gut microbiome may be indicative of certain health conditions, like metabolic syndrome. [21]

CrAss-like phage are thought to be vertically transmitted from mother to offspring, despite the crAss-like phage abundance at birth being low to undetectable. During the first year of life, crAss-like phage abundance and diversity within the gut microbiome significantly increases. [22] Additionally, there is strong evidence that specific crAss-like phage can be transmitted between humans via fecal microbial transplants (FMTs). [22]

The RNA polymerase of crAss-like phage phi14:2 shares structural homology to RNA polymerases used to catalyze RNA interference in humans and animals. Phi14:2 is thought to deliver its RNA polymerase into the host cell upon infection where it can begin transcription of phi14:2 genes. Because of the delivery mechanism and the similarity of eukaryotic RNA interference polymerases and the phi14:2 RNA polymerase, it's hypothesized that eukaryotic RNA interference polymerases may have originated from phage. [23]

Gubaphages have been identified as another highly abundant phage group in the human gut microbiome. The characteristics of the gubaphages are reminiscent to those of p-crAssphage. [24] [25]

crAss-like phage environments

Based on a sequence similarity screen of p-crAssphage protein sequences to protein sequences in public sequence databases and metagenomes, it was concluded that the crAss-like phage family may consist of a wide diversity of bacteriophage members which can be found in a range of environments including human guts and termite guts, terrestrial/groundwater environments, soda lake (hypersaline brine), marine sediment, and plant root environments. [12]

Related Research Articles

<span class="mw-page-title-main">Bacteriophage</span> Virus that infects and replicates within bacteria

A bacteriophage, also known informally as a phage, is a virus that infects and replicates within bacteria and archaea. The term was derived from bacteria and the Ancient Greek word φαγεῖν, meaning 'to devour'. 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">Lambda phage</span> Bacteriophage that infects Escherichia coli

Enterobacteria phage λ is a bacterial virus, or bacteriophage, that infects the bacterial species Escherichia coli. It was discovered by Esther Lederberg in 1950. The wild type of this virus has a temperate life cycle that allows it to either reside within the genome of its host through lysogeny or enter into a lytic phase, during which it kills and lyses the cell to produce offspring. Lambda strains, mutated at specific sites, are unable to lysogenize cells; instead, they grow and enter the lytic cycle after superinfecting an already lysogenized cell.

<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">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">Phage therapy</span> Therapeutic use of bacteriophages to treat bacterial infections

Phage therapy, viral phage therapy, or phagotherapy is the therapeutic use of bacteriophages for the treatment of pathogenic bacterial infections. This therapeutic approach emerged at the beginning of the 20th century but was progressively replaced by the use of antibiotics in most parts of the world after the Second World War. Bacteriophages, known as phages, are a form of virus that attach to bacterial cells and inject their genome into the cell. The bacteria's production of the viral genome interferes with its ability to function, halting the bacterial infection. The bacterial cell causing the infection is unable to reproduce and instead produces additional phages. Phages are very selective in the strains of bacteria they are effective against.

<i>Podoviridae</i> Family of viruses

Podoviridae was a family of bacteriophage in the order Caudovirales often associated with T-7 like phages. The family and order Caudoviraleshave now been abolished, with the term podovirus now used to refer to the morphology of viruses in this former family. There were 130 species in this family, assigned to 3 subfamilies and 52 genera. This family was characterized by having very short, noncontractile tails. Many former phages in the former family Podoviriade are now classified in the Autographiviridae

<span class="mw-page-title-main">CRISPR</span> Family of DNA sequence found in prokaryotic organisms

CRISPR is a family of DNA sequences found in the genomes of prokaryotic organisms such as bacteria and archaea. Each sequence within an individual prokaryotic cell is derived from a DNA fragment of a bacteriophage that had previously infected the prokaryote or one of its ancestors. These sequences are used to detect and destroy DNA from similar bacteriophages during subsequent infections. Hence these sequences play a key role in the antiviral defense system of prokaryotes and provide a form of heritable, acquired immunity. CRISPR is found in approximately 50% of sequenced bacterial genomes and nearly 90% of sequenced archaea.

<i>Bacteroides</i> Genus of bacteria

Bacteroides is a genus of Gram-negative, obligate anaerobic bacteria. Bacteroides species are non endospore-forming bacilli, and may be either motile or nonmotile, depending on the species. The DNA base composition is 40–48% GC. Unusual in bacterial organisms, Bacteroides membranes contain sphingolipids. They also contain meso-diaminopimelic acid in their peptidoglycan layer.

<span class="mw-page-title-main">T7 phage</span> Species of virus

Bacteriophage T7 is a bacteriophage, a virus that infects bacteria. It infects most strains of Escherichia coli and relies on these hosts to propagate. Bacteriophage T7 has a lytic life cycle, meaning that it destroys the cell it infects. It also possesses several properties that make it an ideal phage for experimentation: its purification and concentration have produced consistent values in chemical analyses; it can be rendered noninfectious by exposure to UV light; and it can be used in phage display to clone RNA binding proteins.

<span class="mw-page-title-main">Bacteriophage Qbeta</span> Species of virus

Bacteriophage Qbeta, commonly referred to as Qbeta or Qβ, is a species consisting of several strains of positive-strand RNA virus which infects bacteria that have F-pili, most commonly Escherichia coli. Its linear genome is packaged into an icosahedral capsid with a diameter of 28 nm. Bacteriophage Qβ enters its host cell after binding to the side of the F-pilus.

<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.

In biology, a pathogen, in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a germ.

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

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<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.

<span class="mw-page-title-main">Kill the Winner hypothesis</span> Microbiological population model hypothesis

The "Kill the Winner" hypothesis (KtW) is an ecological model of population growth involving prokaryotes, viruses and protozoans that links trophic interactions to biogeochemistry. The model is related to the Lotka–Volterra equations. It assumes that prokaryotes adopt one of two strategies when competing for limited resources: priority is either given to population growth ("winners") or survival ("defenders"). As "winners" become more abundant and active in their environment, their contact with host-specific viruses increases, making them more susceptible to viral infection and lysis. Thus, viruses moderate the population size of "winners" and allow multiple species to coexist. Current understanding of KtW primarily stems from studies of lytic viruses and their host populations.

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<span class="mw-page-title-main">Cetacean microbiome</span> Group of communities of microorganisms that reside within whales

The cetacean microbiome is the group of communities of microorganisms that reside within whales.

<span class="mw-page-title-main">Phageome</span> Collection of bacteriophages found in a particular environment

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  24. ↑ Camarillo-Guerrero, Luis F.; Almeida, Alexandre; Rangel-Pineros, Guillermo; Finn, Robert D.; Lawley, Trevor D. (2021-02-18). "Massive expansion of human gut bacteriophage diversity". Cell. 184 (4): 1098–1109.e9. doi: 10.1016/j.cell.2021.01.029 . ISSN   0092-8674. PMC   7895897 . PMID   33606979. S2CID   221510077.
  25. ↑ Luis Fernando Camarillo Guerrero: Integrative Analysis of the Human Gut Phageome Using a Metagenomics Approach Archived 2021-02-01 at the Wayback Machine , Thesis, Gonville & Caius College, University of Cambridge, August 2020, doi:10.17863/CAM.63973
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