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ACKNOWLEDGMENTS This research was funded by the Spanish Ministerio de Economia, Industria y Competitividad (MINECO) cofinanced by FEDER funds, grant numbers SAF2017-82287-R and PID2020-118602RB-I00, and the Generalitat Valenciana, grant number AICO/2021/085. We declare no competing interests.

Analysis of institutional authors

Cebria-Mendoza, MariaAuthor

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February 1, 2025
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Human Anelloviruses: Influence of Demographic Factors, Recombination, and Worldwide Diversity

Publicated to:Microbiology Spectrum. 11 (3): e0492822- - 2023-05-18 11(3), DOI: 10.1128/spectrum.04928-22

Authors: Cebria-Mendoza, Maria; Beamud, Beatriz; Andreu-Moreno, Ivan; Arbona, Cristina; Larrea, Luis; Diaz, Wladimiro; Sanjuan, Rafael; Cuevas, Jose M

Affiliations

Ctr Invest Biomed Red Epidemiol & Salud Publ CIBER, Madrid, Spain - Author
Ctr Transfus Comunidad Valenciana, Valencia, Spain - Author
Fdn Promot Sanit & Biomed Res Valencia Reg FISABIO, Genom & Hlth Area, Valencia, Spain - Author
Generalitat Valenciana, FISABIO Salud Publ, Valencia, Spain - Author
Univ Valencia, Dept Genet, Valencia, Spain - Author
Univ Valencia, Inst Integrat Syst Biol I2SysBio, CSIC, Valencia, Spain - Author
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Abstract

Anelloviruses are the most common human infectious viruses and are considered essentially harmless. Compared to other human viruses, they are characterized by enormous diversity, and recombination is suggested to play an important role in their diversification and evolution. Anelloviruses represent the major and most diverse component of the healthy human virome, referred to as the anellome. In this study, we determined the anellome of 50 blood donors, forming two sex- and age-matched groups. Anelloviruses were detected in 86% of the donors. The number of detected anelloviruses increased with age and was approximately twice as high in men as in women. A total of 349 complete or nearly complete genomes were classified as belonging to torque teno virus (TTV), torque teno mini virus (TTMV), and torque teno midi virus (TTMDV) anellovirus genera (197, 88, and 64 sequences, respectively). Most donors had intergenus (69.8%) or intragenus (72.1%) coinfections. Despite the limited number of sequences, intradonor recombination analysis showed 6 intragenus recombination events in ORF1. As thousands of anellovirus sequences have been described recently, we finally analyzed the global diversity of human anelloviruses. Species richness and diversity were close to saturation in each anellovirus genus. Recombination was found to be the main factor promoting diversity, although its effect was significantly lower in TTV than in TTMV and TTMDV. Overall, our results suggest that differences in diversity between genera may be caused by variations in the relative contribution of recombination.IMPORTANCE Anelloviruses are the most common human infectious viruses and are considered essentially harmless. Compared to other human viruses, they are characterized by enormous diversity, and recombination is suggested to play an important role in their diversification and evolution. Here, by analyzing the composition of the plasma anellome of 50 blood donors, we find that recombination is also a determinant of viral evolution at the intradonor level. On a larger scale, analysis of anellovirus sequences currently available in databases shows that their diversity is close to saturation and differs among the three human anellovirus genera and that recombination is the main factor explaining this intergenus variability. Global characterization of anellovirus diversity could provide clues about possible associations between certain virus variants and pathologies, as well as facilitate the implementation of unbiased PCR-based detection protocols, which may be relevant for using anelloviruses as endogenous markers of immune status.

Keywords

AnelloviridaeAnellovirusBlood anellomeDemographyDna virus infectionsDna, viralExtrapolationFemaleHuman viromeHumansMaleMetagenomicsRarefactioRecombinationRecombination, geneticTorque teno virusTorquetenovirusViromVirome

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Microbiology Spectrum due to its progression and the good impact it has achieved in recent years, according to the agency Scopus (SJR), it has become a reference in its field. In the year of publication of the work, 2023, it was in position , thus managing to position itself as a Q1 (Primer Cuartil), in the category Ecology.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 2.53. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Field Citation Ratio (FCR) from Dimensions: 4.74 (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-08, the following number of citations:

  • WoS: 13
  • Europe PMC: 9

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-08:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 14.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 14 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 2.25.
  • The number of mentions on the social network X (formerly Twitter): 3 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: First Author (Cebriá Mendoza, María Concepción) .