TY - JOUR
T1 - A critical analysis of the current state of virus taxonomy
AU - Caetano-Anollés, Gustavo
AU - Claverie, Jean Michel
AU - Nasir, Arshan
N1 - Research has been supported by grants from the National Institute of Food and Agriculture, the Illinois Campus Cluster Program (ICCP), and Blue Waters supercomputing allocations from the National Center for Supercomputing Applications (NCSA) to GC-A, and by recurrent funding from CNRS and Aix-Marseille University (IGS) to C. Abergel and the IGS laboratory.
PY - 2023
Y1 - 2023
N2 - Taxonomical classification has preceded evolutionary understanding. For that reason, taxonomy has become a battleground fueled by knowledge gaps, technical limitations, and a priorism. Here we assess the current state of the challenging field, focusing on fallacies that are common in viral classification. We emphasize that viruses are crucial contributors to the genomic and functional makeup of holobionts, organismal communities that behave as units of biological organization. Consequently, viruses cannot be considered taxonomic units because they challenge crucial concepts of organismality and individuality. Instead, they should be considered processes that integrate virions and their hosts into life cycles. Viruses harbor phylogenetic signatures of genetic transfer that compromise monophyly and the validity of deep taxonomic ranks. A focus on building phylogenetic networks using alignment-free methodologies and molecular structure can help mitigate the impasse, at least in part. Finally, structural phylogenomic analysis challenges the polyphyletic scenario of multiple viral origins adopted by virus taxonomy, defeating a polyphyletic origin and supporting instead an ancient cellular origin of viruses. We therefore, prompt abandoning deep ranks and urgently reevaluating the validity of taxonomic units and principles of virus classification.
AB - Taxonomical classification has preceded evolutionary understanding. For that reason, taxonomy has become a battleground fueled by knowledge gaps, technical limitations, and a priorism. Here we assess the current state of the challenging field, focusing on fallacies that are common in viral classification. We emphasize that viruses are crucial contributors to the genomic and functional makeup of holobionts, organismal communities that behave as units of biological organization. Consequently, viruses cannot be considered taxonomic units because they challenge crucial concepts of organismality and individuality. Instead, they should be considered processes that integrate virions and their hosts into life cycles. Viruses harbor phylogenetic signatures of genetic transfer that compromise monophyly and the validity of deep taxonomic ranks. A focus on building phylogenetic networks using alignment-free methodologies and molecular structure can help mitigate the impasse, at least in part. Finally, structural phylogenomic analysis challenges the polyphyletic scenario of multiple viral origins adopted by virus taxonomy, defeating a polyphyletic origin and supporting instead an ancient cellular origin of viruses. We therefore, prompt abandoning deep ranks and urgently reevaluating the validity of taxonomic units and principles of virus classification.
KW - ICTV
KW - classification
KW - evolution
KW - holobiont
KW - horizontal genetic transfer
KW - reticulation
KW - virus origin
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U2 - 10.3389/fmicb.2023.1240993
DO - 10.3389/fmicb.2023.1240993
M3 - Review article
C2 - 37601376
AN - SCOPUS:85168255837
SN - 1664-302X
VL - 14
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
M1 - 1240993
ER -