The transferome of metabolic genes explored: analysis of the horizontal transfer of enzyme encoding genes in unicellular eukaryotes

AbstractThe subfamily GH13_1 of alpha-amylases is typical of Fungi, but it is also found in some unicellular eukaryotes (e.g. Amoebozoa, choanoflagellates) and non-bilaterian Metazoa. Since a previous study in 2007, GH13_1 amylases were considered ancestral to the Unikonts, including animals, except Bilateria, such that it was thought to have been lost in the ancestor of this clade. The only alpha-amylases known to be present in Bilateria so far belong to the GH13_15 and 24 subfamilies (commonly called bilaterian alpha-amylases) and were likely acquired by horizontal transfer from a proteobacterium. The taxonomic scope of Eukaryota genomes in databases has been greatly increased ever since 2007. We have surveyed GH13_1 sequences in recent data from ca. 1600 bilaterian species, 60 non-bilaterian animals and also in unicellular eukaryotes. As expected, we found a number of those sequences in non-bilaterians: Anthozoa (Cnidaria) and in sponges, confirming the previous observations, but none in jellyfishes and in Ctenophora. Our main and unexpected finding is that such fungal (also called Dictyo-type) amylases were also consistently retrieved in several bilaterian phyla: hemichordates (deuterostomes), brachiopods and related phyla, some molluscs and some annelids (protostomes). We discuss evolutionary hypotheses possibly explaining the scattered distribution of GH13_1 across bilaterians, namely, the retention of the ancestral gene in those phyla only and/or horizontal transfers from non-bilaterian donors.

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Evidence of repeated horizontal transfer of sterol C-5 desaturase encoding genes among dikarya fungi

Molecular Phylogenetics and Evolution ◽

10.1016/j.ympev.2020.106850 ◽

2020 ◽

Vol 150 ◽

pp. 106850 ◽

Cited By ~ 1

Author(s):

Stephanie Herzog ◽

Henner Brinkmann ◽

Miguel Vences ◽

André Fleißner

Keyword(s):

Horizontal Transfer ◽

Encoding Genes

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Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks

Genome Biology ◽

10.1186/s13059-018-1526-x ◽

2018 ◽

Vol 19 (1) ◽

Cited By ~ 2

Author(s):

Daniel Pers ◽

Jeremy A. Lynch

Keyword(s):

Gene Regulatory Networks ◽

Horizontal Transfer ◽

Regulatory Networks ◽

Developmental Gene ◽

Gene Regulatory ◽

Encoding Genes

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Horizontal Transfer and Gene Loss Shaped the Evolution of Alpha-Amylases in Bilaterians

G3 Genes|Genome|Genetics ◽

10.1534/g3.119.400826 ◽

2019 ◽

Vol 10 (2) ◽

pp. 709-719 ◽

Cited By ~ 2

Author(s):

Andrea Desiderato ◽

Marcos Barbeitos ◽

Clément Gilbert ◽

Jean-Luc Da Lage

Keyword(s):

Horizontal Transfer ◽

Gene Loss ◽

Unexpected Finding ◽

Ancestral Gene ◽

Unicellular Eukaryotes ◽

Horizontal Transfers ◽

Alpha Amylases

The subfamily GH13_1 of alpha-amylases is typical of Fungi, but it is also found in some unicellular eukaryotes (e.g., Amoebozoa, choanoflagellates) and non-bilaterian Metazoa. Since a previous study in 2007, GH13_1 amylases were considered ancestral to the Unikonts, including animals, except Bilateria, such that it was thought to have been lost in the ancestor of this clade. The only alpha-amylases known to be present in Bilateria so far belong to the GH13_15 and 24 subfamilies (commonly called bilaterian alpha-amylases) and were likely acquired by horizontal transfer from a proteobacterium. The taxonomic scope of Eukaryota genomes in databases has been greatly increased ever since 2007. We have surveyed GH13_1 sequences in recent data from ca. 1600 bilaterian species, 60 non-bilaterian animals and also in unicellular eukaryotes. As expected, we found a number of those sequences in non-bilaterians: Anthozoa (Cnidaria) and in sponges, confirming the previous observations, but none in jellyfishes and in Ctenophora. Our main and unexpected finding is that such fungal (also called Dictyo-type) amylases were also consistently retrieved in several bilaterian phyla: hemichordates (deuterostomes), brachiopods and related phyla, some molluscs and some annelids (protostomes). We discuss evolutionary hypotheses possibly explaining the scattered distribution of GH13_1 across bilaterians, namely, the retention of the ancestral gene in those phyla only and/or horizontal transfers from non-bilaterian donors.

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Identification of Three Novel Superantigen-Encoding Genes in Streptococcus equi subsp. zooepidemicus, szeF, szeN, and szeP

Infection and Immunity ◽

10.1128/iai.00751-10 ◽

2010 ◽

Vol 78 (11) ◽

pp. 4817-4827 ◽

Cited By ~ 42

Author(s):

Romain Paillot ◽

Alistair C. Darby ◽

Carl Robinson ◽

Nicola L. Wright ◽

Karen F. Steward ◽

...

Keyword(s):

Horizontal Transfer ◽

Mononuclear Cells ◽

Opportunistic Pathogen ◽

Mitogenic Activity ◽

Peripheral Blood Mononuclear ◽

Necrosis Factor Alpha ◽

Streptococcus Equi ◽

Factor Alpha ◽

Encoding Genes

ABSTRACT The acquisition of superantigen-encoding genes by Streptococcus pyogenes has been associated with increased morbidity and mortality in humans, and the gain of four superantigens by Streptococcus equi is linked to the evolution of this host-restricted pathogen from an ancestral strain of the opportunistic pathogen Streptococcus equi subsp. zooepidemicus. A recent study determined that the culture supernatants of several S. equi subsp. zooepidemicus strains possessed mitogenic activity but lacked known superantigen-encoding genes. Here, we report the identification and activities of three novel superantigen-encoding genes. The products of szeF, szeN, and szeP share 59%, 49%, and 34% amino acid sequence identity with SPEH, SPEM, and SPEL, respectively. Recombinant SzeF, SzeN, and SzeP stimulated the proliferation of equine peripheral blood mononuclear cells, and tumor necrosis factor alpha (TNF-α) and gamma interferon (IFN-γ) production, in vitro. Although none of these superantigen genes were encoded within functional prophage elements, szeN and szeP were located next to a prophage remnant, suggesting that they were acquired by horizontal transfer. Eighty-one of 165 diverse S. equi subsp. zooepidemicus strains screened, including 7 out of 15 isolates from cases of disease in humans, contained at least one of these new superantigen-encoding genes. The presence of szeN or szeP, but not szeF, was significantly associated with mitogenic activity in the S. equi subsp. zooepidemicus population (P < 0.000001, P < 0.000001, and P = 0.104, respectively). We conclude that horizontal transfer of these novel superantigens from and within the diverse S. equi subsp. zooepidemicus population is likely to have implications for veterinary and human disease.

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Ankyrin domain encoding genes resulting from an ancient horizontal transfer are functionally integrated into developmental gene regulatory networks in the wasp Nasonia

10.1101/383968 ◽

2018 ◽

Cited By ~ 2

Author(s):

Daniel Pers ◽

Jeremy A. Lynch

Keyword(s):

Horizontal Transfer ◽

Regulatory Networks ◽

Expression Patterns ◽

Functional Integration ◽

Large Family ◽

Novel Genes ◽

Integrated Network ◽

Developmental Networks ◽

Fully Integrated ◽

Encoding Genes

ABSTRACTBackgroundHow and why regulatory networks incorporate additional components, and how novel genes are maintained and functionally integrated into developmental processes are two important and intertwined questions whose answers have major implications for the evolution of development. We recently described a set of novel genes with robust and unique expression patterns along the dorsal-ventral axis of the embryo of the wasp Nasonia. Given the unique evolutionary history of these genes, and their apparent integration in to the dorsal-ventral (DV) patterning network, they are collectively an excellent model to study the evolution of regulatory networks, and the fates of novel genes.ResultsWe have found that the novel DV genes are part of a large family of rapidly duplicating and diverging ankyrin domain encoding genes that originated most likely by horizontal transfer from Wolbachia in a common ancestor of the wasp superfamilly Chalcidoidea. We tested the function of those ankyrin encoding genes expressed along the DV axis and found that they participate in early embryonic DV patterning. We also developed a new wasp model system (Melittobia) and found that some functional integration of ankyrin genes have been preserved for over 90 million years, while others are lineage specific.ConclusionsOur results indicate that regulatory networks can incorporate novel genes that then become necessary for stable and repeatable outputs. Even modest role in developmental networks may be enough to allow novel or duplicate genes to be maintained in the genome and become fully integrated network components.

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