Successive Losses of Central Immune Genes Characterize the Gadiformes’ Alternate Immunity

Abstract

Great genetic variability among teleost immunomes, with gene losses and expansions of central adaptive and innate components, has been discovered through genome sequencing over the last few years. Here, we demonstrate that the innate Myxovirus resistance gene (Mx) is lost from the ancestor of Gadiformes and the closely related Stylephorus chordatus, thus predating the loss of Major Histocompatibility Complex class II (MHCII) in Gadiformes. Although the functional implication of Mx loss is still unknown, we demonstrate that this loss is one of several ancient events appearing in successive order throughout the evolution of teleost immunity. In particular, we find that the loss of Toll-like receptor 5 predates the loss of Mx involving the entire Paracanthopterygii lineage. Using a time-calibrated phylogeny, we show that loss of MHCII and Mx overlap with major paleoclimatic and geological events indicating that these genetic changes were adaptive responses to the changing environment at the time.

The Phylogenetic Intrarelationships of Spiny-Rayed Fishes (Acanthomorpha, Teleostei, Actinopterygii): Fossil Taxa Increase the Congruence of Morphology with Molecular Data

“…The first molecular (mitogenomic) phylogenetic analysis that includes this species (Miya et al, 2007) proposed a different position for Stylephorus, within the Gadiformes-Zeiformes clade ( Figure 1B). This result has been corroborated subsequently in every other analysis of mitochondrial and nuclear markers (Near et al, 2012(Near et al, , 2013Betancur-R et al, 2013;Grande et al, 2013;Malmstrøm et al, 2016), and by the shared loss of the immune system's Mx gene (Solbakken et al, 2016). This new arrangement has also been supported (Grande et al, 2013) and opposed (Roberts, 2012) on the basis of morphology, each time without a comprehensive phylogenetic analysis.…”

Transcriptome-wide mapping of signaling pathways and early immune responses in lumpfish leukocytes upon in vitro bacterial exposure

“…Fish and amphibians also have a soluble version of TLR5, termed TLR5S 6 in addition to a membrane bound TLR5 (TLR5M). TLR5 has been identified in all investigated teleost species, with the exception of the Paracanthopterygii 7 . From functional studies and functional inference based on sequence homology indicate that fish TLR1, TLR2, TLR5, TLR5S, TLR9, TLR21, TLR28 5 , 8 , 9 recognize bacterial ligands.…”

Genomic architecture of haddock (Melanogrammus aeglefinus) shows expansions of innate immune genes and short tandem repeats

“…Additionally, other immune related genes have likely been lost prior to this event, e.g. the Toll-like receptor ( TLR ) 5 151–147 million years ago and the Myxovirus resistance gene ( Mx ) 126–104 million years ago [ 13 ]. A detailed characterization of the TLR gene repertoire – membrane-bound receptors belonging to the pattern recognition receptors (PRRs) family and an important component of the innate immunity [ 14 ] – within the Gadiformes lineage revealed specific losses and several expansions [ 12 , 15 ].…”