Biology subjects

Lavrov, D. V.

Publications and source records attributed to Lavrov, D. V..

11 recordsLinked to original sources

bioRxiv2025

Hidden in Plain Sight: A Novel Symbiotic Haplosclerid Sponge Species Revealed by its Mitochondrial Genome

An unusual third mitochondrial genome was discovered in the genomic data from the symbiotic association between two sponges, Haliclona plakophila (Haplosclerida, Demospongiae) and Plakortis symbiotica (Homoscleromorpha). This mitogenome exhibited an unusually high GC content, lacked the cox2 gene, and could not be reliably positioned among animals based on phylogenetic analysis of the sequence data. Nevertheless, conserved gene clusters and the presence of atp9 indicated that this species is a sponge, while phylogenetic analysis using 18S and 28S places it in the order Haplosclerida of Demospongiae. Since no tissue of the cryptic sponge was found in the investigated association, its relationship with other sponges remained unclear. Therefore, we sampled 10 additional samples assumed to be H. plakophila - P. symbiotica associations in the field to search for the mysterious third sponge. PCR analysis revealed that one of the collected samples contained the novel sponge, but not H. plakophila. A follow-up morphological investigation revealed that this sponge, Haplosclerida sp. nov., while superficially indistinguishable from H. plakophila, differs in skeletal organization and spicule composition. Here, we report the unusual mitochondrial genome of the new species, along with a phylogenetic analysis using 18S and 28S sequences, and demonstrate that Haplosclerida sp. nov. belongs to a new clade of Haplosclerida. We also report the mitogenome of Xestospongia deweerdtae, another haplosclerid species described in association with multiple Plakortis species, including P. symbiotica. Our results support multiple origins of Haplosclerida-Plakortis symbiosis and open new avenues for its investigation.

evolutionary biology↗

bioRxiv2024

Expansion of the MutS gene family in plants

The MutS gene family is distributed across the tree of life and is involved in recombination, DNA repair, and protein translation. Multiple evolutionary processes have expanded the set of MutS genes in plants relative to other eukaryotes. Here, we investigate the origins and functions of these plant-specific genes. Land plants, green algae, red algae, and glaucophytes share cyanobacterial-like MutS1 and MutS2 genes that presumably were gained via plastid endosymbiotic gene transfer. MutS1 was subsequently lost in some taxa, including seed plants, whereas MutS2 was duplicated in Viridiplantae (i.e., land plants and green algae) with widespread retention of both resulting paralogs. Viridiplantae also have two anciently duplicated copies of the eukaryotic MSH6 gene (i.e., MSH6 and MSH7) and acquired MSH1 via horizontal gene transfer - potentially from a nucleocytovirus. Despite sharing the same name, "plant MSH1" is not directly related to the gene known as MSH1 in some fungi and animals, which may be an ancestral eukaryotic gene acquired via mitochondrial endosymbiosis and subsequently lost in most eukaryotic lineages. There has been substantial progress in understanding the functions of MSH1 and MSH6/MSH7 in plants, but the roles of the cyanobacterial-like MutS1 and MutS2 genes remain uncharacterized. Known functions of bacterial homologs and predicted protein structures, including fusions to diverse nuclease domains, provide hypotheses about potential molecular mechanisms. Because most plant-specific MutS proteins are targeted to the mitochondria and/or plastids, the expansion of this family appears to have played a large role in shaping plant organelle genetics. One-Sentence SummaryPlants are distinguished from other eukaryotes by a functionally diverse complement of MutS proteins gained via a combination of gene duplication, endosymbiotic gene transfer, and horizontal gene transfer.

evolutionary biology↗

bioRxiv2024

Pervasive mitochondrial tRNA gene loss in the clade B of haplosclerid sponges (Porifera, Demospongiae).

AbstractMitochondrial tRNA gene loss and cytosolic tRNA import to mitochondria are two common phenomena in mitochondrial biology, but their importance is often under-appreciated in animals. This is because most bilaterally symmetrical animals (Bilateria) encode a complete set of tRNAs needed for mitochondrial translation. By contrast, studies of mitochondrial genomes in non-bilaterian animals have shown a reduced tRNA gene content in several lineages, necessitating tRNA import. Interestingly, in most of these lineages tRNA gene content appears to be set early in the evolution of the group and conserved thereafter. Here we demonstrate that Clade B of Haplosclerid Sponges (CBHS) represent an exception to this pattern. We determined mt-genome sequences for eight species from this group and analyzed them with six that had been previously available. In addition, we determined mt-genome sequences for two species of haploslerid sponges outside the CBHS and used them with eight previously available sequences as outgroups. We found that tRNA gene content varied widely among CBHS species: from three in an undescribed Haliclona species (Haliclona sp. TLT785) to 25 in Xestospongia muta and X. testudinaria. Furthermore, we found that all CBHS species outside the genus Xestospongia lacked atp9, while some also lacked atp8. Analysis of nuclear sequences from Niphates digitalis revealed that both atp8 and atp9 had transferred to the nuclear genome, while the absence of mt-tRNA genes represented their genuine loss. Overall, CBHS can be a useful animal system to study mt-tRNA genes loss, mitochondrial import of cytosolic tRNA, and the impact of both of these processes on mitochondrial evolution. Significance statementIt is generally believed that the gene content is stable in animal mitochondrial (mt) DNA. Indeed, mtDNA in most bilaterally symmetrical animals encompasses a conserved set of 37 genes coding for 13 proteins, two rRNAs and 22 tRNAs. By contrast, mtDNA in non-bilaterian animals shows more variation in mt gene content, in particular in the number of tRNA genes. However, most of this variation occurs between major non-bilaterian lineages. Here we demonstrate that a group of demosponges called Clade B of Haplosclerid Sponges (CBHS) represents a fascinating exception to this pattern, with species experiencing recurrent losses of up to 22 mt-tRNA genes. We argue that this group constitutes a promising system to investigate the effects of tRNA gene loss on evolution of mt-genomes as well as mitochondrial tRNA import machinery.

evolutionary biology↗

bioRxiv2024

Acanthella acuta Mitochondrial DNA: Linear Architecture and Other Unique Features

While Acanthella acuta (Schmidt 1862), a common demosponge found in the Mediterranean Sea and Atlantic Ocean, is -- morphologically -- little distinguishable from other sponges, its mitochondrial DNA (mtDNA) is unique within the class. In contrast to all other studied demosponges, A. acuta mtDNA appears to be linear and displays several unusual features: inverted terminal repeats, group II introns in three mt-genes, and two unique ORFs. One of the ORFs (ORF1535) combines a DNA-polymerase domain with a DNA-directed RNA-polymerase domain, while the second bears no discernable similarity to any reported sequences. The group II intron within the cox2 gene is the first such intron reported in an animal. Our phylogenetic analyses indicate that the cox1 intron is related to similar introns found in other demosponges, while the cox2 intron is likely not of animal origin. The two domains found within ORF1535 do not share a common origin and, along with the cox2 intron, were likely acquired by horizontal transfer. The findings of this paper open new avenues of exploration in the understanding of mtDNA linearization within Metazoa. SignificanceThe transition from circular to linear mtDNA architecture is a rare and poorly understood phenomenon in animals. In addition, the few lineages that made this transition (Medusozoa, Calcarea, and Isopoda), adopted linear mt-DNA architecture early in their history, making it difficult to reconstruct the underlying events. The identification of linear mtDNA in Acanthella acuta not only provides an independent example of the origin of linear mtDNA architectures in animals but also an opportunity to investigate its evolution at a much shorter evolutionary time. In particular, the conservation of circular mtDNA in other studied species within the family Dictyonellidae highlights the need to investigate other species in the genus Acanthella, to better understand mtDNA linearization in A. acuta.

evolutionary biology↗

bioRxiv2023

Characterization of the mitochondrial proteome in the ctenophore Mnemiopsis leidyi using MitoPredictor

ii.Mitochondrial proteomes have been experimentally characterized for only a handful of animal species. However, the increasing availability of genomic and transcriptomic data allows one to infer mitochondrial proteins using computational tools. MitoPredictor is a novel random-forest classifier, which utilizes orthology-search, mitochondrial targeting signal (MTS) identification, and protein domain content to infer mitochondrial proteins in animals. MitoPredictors output also includes an easy-to-use R Shiny applet for the visualization and analysis of the results. In this article, we provide a guide for predicting and analyzing the mitochondrial proteome of the ctenophore Mnemiopsis leidyi using MitoPredictor.

bioinformatics↗

bioRxiv2023

Phylomitogenomics bolsters the high-level classification of Demospongiae (phylum Porifera)

Class Demospongiae - the largest in the phylum Porifera (Sponges) - encompasses nearly 8,000 accepted species in three subclasses: Keratosa, Verongimorpha, and Heteroscleromorpha. Subclass Heteroscleromorpha contains [~]90% of demosponge species and is subdivided into 17 orders. The higher level classification of demosponges underwent major revision as the result of nearly three decades of molecular studies. However, because most of the previous molecular work only utilized partial data from a small number of nuclear and mitochondrial (mt) genes, this classification scheme needs to be tested by larger datasets. Here we compiled a mt dataset for 136 demosponge species - including 64 complete or nearly complete and six partial mt-genome sequences determined or assembled for this study - and used it to test phylogenetic relationships among Demospongiae in general and Heteroscleromorpha in particular. We also investigated the phylogenetic position of Myceliospongia araneosa - a highly unusual demosponge without spicules and spongin fibers, currently classified as Demospongiae incertae sedis, for which molecular data were not available. Our results support the previously inferred sister-group relationship between Heteroscleromorpha and Keratosa + Verongimorpha and suggest five main clades within Heteroscleromorpha: Clade C0 composed of order Haplosclerida; Clade C1 composed of Scopalinida, Sphaerocladina, and Spongillida; Clade C2 composed of Axinellida, Biemnida, Bubarida; Clade C3 composed of Tetractinellida; and Clade C4 composed of Agelasida, Clionaida, Desmacellida, Merliida, Suberitida, Poecilosclerida, Polymastiida, and Tethyida. The inferred relationships among these clades were (C0(C1(C2(C3+C4)))). Analysis of molecular data from M. araneosa placed it in the C3 clade as a sister taxon to the highly skeletonized tetractinellids Microscleroderma sp. and Leiodermatium sp. Molecular clock analysis dated divergences among the major clades in Heteroscleromorpha from the Cambrian to the Early Silurian, the origins of most heteroscleromorph orders in the middle Paleozoic, and the most basal splits within these orders around the Paleozoic to Mesozoic transition. Overall, the results of this study are mostly congruent with the accepted classification of Heteroscleromorpha, but add temporal perspective and new resolution to phylogenetic relationships within this subclass.

evolutionary biology↗

bioRxiv2021

Large dataset of octocoral mitochondrial genomes provides new insights into mt-mutS evolution and function

All studied octocoral mitochondrial genomes contain a gene from the MutS family, whose members code for proteins involved in DNA mismatch repair, other types of DNA repair, meiotic recombination, and other functions. Although mutS homologues are found in all domains of life as well as viruses, octocoral mt-mutS is the only such gene encoded in an organellar genome. While the function of mtMutS is not known, its domain architecture, conserved sequence, and presence of some characteristic residues suggest its involvement in mitochondrial DNA repair. This inference is supported by exceptionally low rates of mt-sequence evolution observed in octocorals. Previous studies of mt-mutS have been limited by the small number of octocoral mt-genomes available. We utilized sequence-capture data from the recent Quattrini et al. study to assemble complete mitochondrial genomes for 97 species of octocorals. Combined with sequences publicly available in GenBank, this resulted in a dataset of 184 complete mitochondrial genomes, which we used to re-analyze the conservation and evolution of mt-mutS. We discovered the first case of mt-mutS loss among octocorals in one of the two Pseudoanthomastus sp. assembled from Quattrini et al. data. This species displayed accelerated rate and and changed patterns of nucleotide substitutions in mt-genome, which we argue provide additional evidence for the role of mtMutS in DNA repair. In addition, we found accelerated mt-sequence evolution in the presence of mt-mutS in several octocoral lineages. This accelerated evolution did not appear to be the result of relaxed selection pressure and did not entail changes in patterns of nucleotide substitutions. Overall, our results support previously reported patterns of conservation in mt-mutS and suggest that mtMutS is involved in DNA repair in octocoral mitochondria. They also indicate that the presence of mt-mutS contributes to, but does not fully explain, the low rates of sequence evolution in octocorals

bioinformatics↗

bioRxiv2020

Dynamic evolution of the MutS family in animals: multiple losses of MSH paralogues and gain of a viral MutS homologue in octocorals

MutS is a key component of the Mismatch Repair (MMR) pathway. Members of the MutS family of proteins are present in bacteria, archaea, eukaryotes, and viruses. Six MutS homologues (MSH1-6), have been identified in yeast, three of which function in nuclear MMR, while MSH1 has been associated with mitochondrial DNA repair. MSH1 is believed to be lacking in animals, potentially reflecting the loss of MMR in animal mitochondria, and correlated with higher rates of mitochondrial sequence evolution. An intriguing exception has been found in octocorals, a group of marine animals from phylum Cnidaria, which encode a MutS-homologue (mtMutS) in their mitochondrial genome. It has been suggested that this protein functions in mitochondrial DNA repair, which would explain some of the lowest rates of mitochondrial sequence evolution observed in this group. To place the acquisition of mtMutS in a functional context, we investigated the evolution of the whole MutS family in animals. Our study confirmed the acquisition of octocoral mtMutS by horizontal gene transfer from a giant virus. Surprisingly, we found orthologues of yeast MSH1 in all hexacorals (the sister group of octocorals) and several sponges and placozoans. By contrast, MSH1 orthologues were lacking in octocorals, medusozoan cnidarians, ctenophores, and bilaterian animals. Furthermore, while we were able to identify MSH2 and MSH6 in all animals, MSH4, MSH5, and, especially, MSH3 were missing in multiple species. Overall, our analysis reveals a dynamic evolution of MSH family in animals, with multiple losses of MSH1, MSH3, some losses of MSH4 and MSH5, and a gain of octocoral mtMutS.

bioinformatics↗

bioRxiv2019

Causes and consequences of mitochondrial proteome size-variation in animals

Despite a conserved set of core mitochondrial functions, animal mitochondrial proteomes show a large variation in size. In this study, we analyzed the putative mechanisms behind and functional significance of this variation using experimentally-verified mt-proteomes of four bilaterian animals and two non-animal outgroups. We found that, of several factors affecting mitochondrial proteome size, evolution of novel mitochondrial proteins in mammals and loss of ancestral proteins in protostomes were the main contributors. Interestingly, gain and loss of conventional mitochondrial targeting signals was not a significant factor in the proteome size evolution.

bioinformatics↗

bioRxiv2019

Phylogenetic relationships of heteroscleromorph demosponges and the affinity of the genus Myceliospongia (Demospongiae incertae sedis)

Class Demospongiae - the largest in the phylum Porifera (Sponges) - encompasses 7,581 accepted species across the three recognized subclasses: Keratosa, Verongimorpha, and Heteroscleromorpha. The latter subclass contains the majority of demosponge species and was previously subdivided into subclasses Heteroscleromorpha sensu stricto and Haploscleromorpha. The current classification of demosponges is the result of nearly three decades of molecular studies that culminated in a formal proposal of a revised taxonomy (Morrow and Cardenas, 2015). However, because most of the molecular work utilized partial sequences of nuclear rRNA genes, this classification scheme needs to be tested by additional molecular markers. Here we used sequences and gene order data from complete or nearly complete mitochondrial genomes of 117 demosponges (including 60 new sequences determined for this study and 6 assembled from public sources) and three additional partial mt-genomes to test the phylogenetic relationships within demosponges in general and Heteroscleromorpha sensu stricto in particular. We also investigated the phylogenetic position of Myceliospongia araneosa - a highly unusual demosponge without spicules and spongin fibers, currently classified as Demospongiae incertae sedis.\n\nOur results support the sub-class relationship within demosponges and reveal four main clades in Heteroscleromorpha sensu stricto: Clade 1 composed of Spongillida, Sphaerocladina, and Scopalinida; Clade 2 composed of Axinellida, Biemnida, Bubarida; Clade 3 composed of Tetractinellida and \"Rhizomorina\" lithistids; and Clade 4 composed of Agelasida, Polymastida, Clionaida, Suberitida, Poecilosclerida, and Tethyida. The four clades appear to be natural lineages that unite previously defined taxonomic orders. Therefore, if those clades are to be systematically interpreted, they will have the rank of superorders (hence S1-S4). We inferred the following relationships among the newly defined clades: (S1(S2(S3+S4))). Analysis of molecular data from Myceliospongia araneosa - first from this species/genus - placed it in S3 as a sister group to Microscleroderma sp. and Leiodermatium sp. (\"Rhizomorina\").\n\nMolecular clock analysis indicated that the origin of the Heteroscleromorpha sensu stricto as well as the basal split in this group between S1 and the rest of the superorder go back to Cambrian, while the divergences among the three other superorders occurred in Ordovician (with the 95% standard variation from Late Cambrian to Early Silurian). Furthermore most of the proposed orders within Heteroscleromorpha appear to have middle Paleozoic origin, while crown groups within order date mostly to Paleozoic to Mesozoic transition. We propose that these molecular clock estimates can be used to readjust ranks for some of the higher taxa within Heteroscleromorpha.\n\nIn addition to phylogenetic information, we found several unusual mtgenomic features among the sampled species, broadening our understanding of mitochondrial genome evolution in this group and animals in general. In particular, we found mitochondrial introns within cox2 (first in animals) and rnl (first in sponges).

genomics↗

bioRxiv2017

Transcriptome sequencing and delimitation of cryptic Oscarella species (O. carmela and O. pearsei sp. nov) from California, USA.

The homoscleromorph sponge Oscarella carmela, first described from central California, USA is shown to represent two morphologically similar but phylogenetically distant species that are co-distributed. We here describe a new species as Oscarella pearsei, sp. nov. and redescribe Oscarella carmela; the original description was based upon material from both species. Further, we correct the identification of published genomic/transcriptomic resources that were originally attributed to O. carmela, and present new Illumina-sequenced transcriptome assemblies for each of these species, and the mitochondrial genome sequence for O. pearsei sp. nov. Using SSU and LSU ribosomal DNA and the mitochondrial genome, we report the phylogenetic relationships of these species relative to other Oscarella species, and find strong support for placement of O. pearsei sp. nov. in a clade defined by the presence of spherulous cells that contain paracrystalline inclusions; O. carmela lacks this cell type and is most closely related to the Western Pacific species, O. malakhovi. Oscarella pearsei sp. nov and O. carmela can be tentatively distinguished based upon gross morphological differences such as color, surface texture and extent of mucus production, but can be more reliably identified using mitochondrial and nuclear barcode sequencing, ultrastructural characteristics of cells in the mesohyl, and the morphology of the follicle epithelium which surrounds the developing embryo in reproductively active individuals. Usually, cryptic species are very closely related to each other, but in this case and in sponges generally, cryptic species may be very distantly related because sponges can be difficult to identify based upon gross morphological characteristics.

evolutionary biology↗