Abstract:Transposable elements are important residents of eukaryotic genomes and eventually
the host can domesticate them to serve cellular functions. We reported here a
possible domestication event of the vestigial interposed retroelement (VIPER) in
trypanosomatids. We found a large gene in a syntenic location in Leishmania
braziliensis, L. panamensis, Leptomanas
pyrrhocoris, and Crithidia fasciculata whose products
share similarity in the C-terminal portion with the third protein of VIPER. No
remnants of other VIPER … Show more
“…The maximum likelihood and Bayesian phylogenomic trees inferred using the supermatrix of 410 proteins encoded by single-copy genes have the same topology and demonstrate maximal supports for almost all branches ( Figure 1 ). This topology is compatible with those inferred previously [ 2 , 9 , 96 , 97 ], which confirms the position of the genera Endotrypanum and Porcisia as the closest known relatives of the genus Leishmania .…”
While numerous genomes of Leishmania spp. have been sequenced and analyzed, an understanding of the evolutionary history of these organisms remains limited due to the unavailability of the sequence data for their closest known relatives, Endotrypanum and Porcisia spp., infecting sloths and porcupines. We have sequenced and analyzed genomes of three members of this clade in order to fill this gap. Their comparative analyses revealed only minute differences from Leishmaniamajor genome in terms of metabolic capacities. We also documented that the number of genes under positive selection on the Endotrypanum/Porcisia branch is rather small, with the flagellum-related group of genes being over-represented. Most significantly, the analysis of gene family evolution revealed a substantially reduced repertoire of surface proteins, such as amastins and biopterin transporters BT1 in the Endotrypanum/Porcisia species when compared to amastigote-dwelling Leishmania. This reduction was especially pronounced for δ-amastins, a subfamily of cell surface proteins crucial in the propagation of Leishmania amastigotes inside vertebrate macrophages and, apparently, dispensable for Endotrypanum/Porcisia, which do not infect such cells.
“…The maximum likelihood and Bayesian phylogenomic trees inferred using the supermatrix of 410 proteins encoded by single-copy genes have the same topology and demonstrate maximal supports for almost all branches ( Figure 1 ). This topology is compatible with those inferred previously [ 2 , 9 , 96 , 97 ], which confirms the position of the genera Endotrypanum and Porcisia as the closest known relatives of the genus Leishmania .…”
While numerous genomes of Leishmania spp. have been sequenced and analyzed, an understanding of the evolutionary history of these organisms remains limited due to the unavailability of the sequence data for their closest known relatives, Endotrypanum and Porcisia spp., infecting sloths and porcupines. We have sequenced and analyzed genomes of three members of this clade in order to fill this gap. Their comparative analyses revealed only minute differences from Leishmaniamajor genome in terms of metabolic capacities. We also documented that the number of genes under positive selection on the Endotrypanum/Porcisia branch is rather small, with the flagellum-related group of genes being over-represented. Most significantly, the analysis of gene family evolution revealed a substantially reduced repertoire of surface proteins, such as amastins and biopterin transporters BT1 in the Endotrypanum/Porcisia species when compared to amastigote-dwelling Leishmania. This reduction was especially pronounced for δ-amastins, a subfamily of cell surface proteins crucial in the propagation of Leishmania amastigotes inside vertebrate macrophages and, apparently, dispensable for Endotrypanum/Porcisia, which do not infect such cells.
“…Previously, this species was classified in the subgenus Sauroleishmania but was later shown from molecular phylogenetics to be closer to members of the Leishmania subgenus 43 , 44 . Leishmania enriettii from the subgenus Mundinia is located between the Viannia and Leishmania subgenera, as inferred by other phylogenetic studies 45 – 47 . However phylogenetic analyses, including other members of Mundinia, such as L. ( Mundinia ) martiniquensis and L. (M.) macropodum, support the most basal position of this subgenus in the genus Leishmania 33 – 35 .…”
The increasing number of available genomic data allowed the development of phylogenomic analytical tools. Current methods compile information from single gene phylogenies, whether based on topologies or multiple sequence alignments. Generally, phylogenomic analyses elect gene families or genomic regions to construct phylogenomic trees. Here, we presented an alternative approach for Phylogenomics, named TOMM (Total Ortholog Median Matrix), to construct a representative phylogram composed by amino acid distance measures of all pairwise ortholog protein sequence pairs from desired species inside a group of organisms. The procedure is divided two main steps, (1) ortholog detection and (2) creation of a matrix with the median amino acid distance measures of all pairwise orthologous sequences. We tested this approach within three different group of organisms: Kinetoplastida protozoa, hematophagous Diptera vectors and Primates. Our approach was robust and efficacious to reconstruct the phylogenetic relationships for the three groups. Moreover, novel branch topologies could be achieved, providing insights about some phylogenetic relationships between some taxa.
“…Several other species presented degenerate copies of VIPER. In L. braziliensis, L. panamensis and L. peruviana, which are three closely related species [40,41], one of the significant hits corresponds to a VIPER-derived gene that was already reported [42].…”
Section: Viper and Tate Present A Discontinuous Distribution In Trypamentioning
Background
Kinetoplastids are a flagellated group of protists, including some parasites, such as
Trypanosoma
and
Leishmania
species, that can cause diseases in humans and other animals. The genomes of these species enclose a fraction of retrotransposons including
VIPER
and
TATE
, two poorly studied transposable elements that encode a tyrosine recombinase (YR) and were previously classified as DIRS elements. This study investigated the distribution and evolution of
VIPER
and
TATE
in kinetoplastids to understand the relationships of these elements with other retrotransposons.
Results
We observed that
VIPER
and
TATE
have a discontinuous distribution among Trypanosomatidae, with several events of loss and degeneration occurring during a vertical transfer evolution. We were able to identify the terminal repeats of these elements for the first time, and we showed that these elements are potentially active in some species, including
T. cruzi
copies of
VIPER
. We found that
VIPER
and
TATE
are strictly related elements, which were named in this study as
VIPER-like
. The reverse transcriptase (RT) tree presented a low resolution, and the origin and relationships among YR groups remain uncertain. Conversely, for RH,
VIPER-like
grouped with
Hepadnavirus
, whereas for YR,
VIPER-like
sequences constituted two different clades that are closely allied to
Crypton
. Distinct topologies among RT, RH and YR trees suggest ancient rearrangements/exchanges in domains and a modular pattern of evolution with putative independent origins for each ORF.
Conclusions
Due to the presence of both elements in
Bodo saltans,
a nontrypanosomatid species, we suggested that
VIPER
and
TATE
have survived and remained active for more than 400 million years or were reactivated during the evolution of the host species. We did not find clear evidence of independent origins of
VIPER-like
from the other YR retroelements, supporting the maintenance of the DIRS group of retrotransposons. Nevertheless, according to phylogenetic findings and sequence structure obtained by this study and other works, we proposed separating DIRS elements into four subgroups:
DIRS-like, PAT-like, Ngaro-like,
and
VIPER-like.
Electronic supplementary material
The online version of this article (10.1186/s13100-019-0175-2) contains supplementary material, which is available to authori...
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