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Integrative taxonomy of a new Redudasys species (Gastrotricha: Macrodasyida) sheds light on the invasion of fresh water habitats by macrodasyids.

ABSTRACT: The order Macrodasyida (Gastrotricha) includes over 350 marine species, and only 3 freshwater species (Marinellina flagellata, Redudasys fornerise, R. neotemperatus). Herein we describe a new freshwater species of Macrodasyida, Redudasys brasiliensis sp. nov., from Brazil through an integrative taxonomic approach. The external morphology and internal anatomy were investigated using differential interference contrast microscopy, confocal microscopy, scanning and transmission electron microscopy. The systematization of the new taxon was inferred by nuclear (18S and 28S) and mitochondrial (COI) genes, and its intra-order relationships were assessed using data from most of available macrodasyids. Phylogenetic analyses yielded congruent trees, in which the new taxon is nested within the family Redudasyidae, but it was genetically distinct from the other species of the genus Redudasys. The new species shares the gross morphology and reproductive traits with other Redudasyidae and the presence of only 1 anterior adhesive tube per side with Redudasys neotemperatus, but it has a specific pattern of ventral ciliation and muscle organization. Results support the hypothesis that dispersion into fresh water habitats by Macrodasyida and Chaetonotida taxa occurred independently and that within Macrodasyida a single lineage invaded the freshwater environment only once. Furthermore, the Neotropical region seems to be peculiar for the evolution of the freshwater macrodasyid clade.

SUBMITTER: Garraffoni ARS

PROVIDER: S-EPMC6376054 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundPhylogenetic relationships within Gastrotricha are poorly known. Attempts to shed light on this subject using morphological traits have led to hypotheses lacking satisfactory statistical support; it seemed therefore that a different approach was needed.Methodology/principal findingsIn this paper we attempt to elucidate the relationships within the taxonomically vast family Thaumastodermatidae (Macrodasyida) using molecular sequence data. The study includes representatives of all the extant genera of the family and for the first time uses a multi-gene approach to infer evolutionary liaisons within Gastrotricha. The final data set comprises sequences of three genes (18S, 28S rDNA and COI mtDNA) from 41 species, including 29 thaumastodermatids, 11 non-thaumastodermatid macrodasyidans and a single chaetonotidan. Molecular data was analyzed as a combined set of 3 genes and as individual genes, using Bayesian and maximum likelihood approaches. Two different outgroups were used: Xenotrichula intermedia (Chaetonotida) and members of the putative basal Dactylopodola (Macrodasyida). Thaumastodermatidae and all other sampled macrodasyidan families were found monophyletic except for Cephalodasyidae. Within Thaumastodermatidae Diplodasyinae and Thaumastodermatinae are monophyletic and so are most genera. Oregodasys turns out to be the most basal group within Thaumastodermatinae in analyses of the concatenated data set as well as in analyses of the nuclear genes. Thaumastoderma appears as the sister taxon to the remaining species. Surprisingly, Tetranchyroderma is non-monophyletic in our analyses as one group of species clusters with Ptychostomella while another appears as the sister group of Pseudostomella.Conclusions/significanceResults in general agree with the current classification; however, a revision of the more derived thaumastodermatid taxa seems necessary. We also found that the ostensible COI sequences from several species do not conform to the general invertebrate or any other published mitochondrial genetic code; they may be mitochondrially derived nuclear genes (numts), or one or more modifications of the mitochondrial genetic code within Gastrotricha.

Project description:Extreme acidophiles thrive in environments rich in protons (pH values <3) and often high levels of dissolved heavy metals. They are distributed across the three domains of the Tree of Life including members of the Proteobacteria. The Acidithiobacillia class is formed by the neutrophilic genus Thermithiobacillus along with the extremely acidophilic genera Fervidacidithiobacillus, Igneacidithiobacillus, Ambacidithiobacillus, and Acidithiobacillus. Phylogenomic reconstruction revealed a division in the Acidithiobacillia class correlating with the different pH optima that suggested that the acidophilic genera evolved from an ancestral neutrophile within the Acidithiobacillia. Genes and mechanisms denominated as "first line of defense" were key to explaining the Acidithiobacillia acidophilic lifestyle including preventing proton influx that allows the cell to maintain a near-neutral cytoplasmic pH and differ from the neutrophilic Acidithiobacillia ancestors that lacked these systems. Additional differences between the neutrophilic and acidophilic Acidithiobacillia included the higher number of gene copies in the acidophilic genera coding for "second line of defense" systems that neutralize and/or expel protons from cell. Gain of genes such as hopanoid biosynthesis involved in membrane stabilization at low pH and the functional redundancy for generating an internal positive membrane potential revealed the transition from neutrophilic properties to a new acidophilic lifestyle by shaping the Acidithiobacillaceae genomic structure. The presence of a pool of accessory genes with functional redundancy provides the opportunity to "hedge bet" in rapidly changing acidic environments. Although a core of mechanisms for acid resistance was inherited vertically from an inferred neutrophilic ancestor, the majority of mechanisms, especially those potentially involved in resistance to extremely low pH, were obtained from other extreme acidophiles by horizontal gene transfer (HGT) events.

Project description:BackgroundGastrotricha systematics is in a state of flux mainly due to the conflicts between cladistic studies base on molecular markers and the classical systematisation based on morphological traits. In sandy samples from Thailand, we found numerous macrodasyidan gastrotrichs belonging to an undescribed species of difficult taxonomic affiliation. The abundance and original nature of the specimens prompted us to undertake a deep survey of both morphological and molecular traits aiming at a reliable systematisation of the new taxon.Methodology/principal findingsUsing several microscopical techniques we investigated the external and internal anatomy, including the muscular and nervous systems of the new species. Additional specimens were used to obtain the 18S rRNA gene sequence; molecular data was analysed cladistically in conjunction with data from additional species belonging to the near complete Macrodasyida taxonomic spectrum. Specimens are vermiform, up to 806 μm in total length, and show a well-defined head equipped with peculiar leaf-like sensorial organs and a single-lobed posterior end. The adhesive apparatus includes anterior, ventrolateral, dorsal and posterior tubes. Pharynx is about 1/4 of the total length and shows pores at its posterior 3/4. Adult specimens exhibit maturing eggs and a bulky, muscular caudal organ, but do not show sperm nor the frontal organ. Musculature and nervous system organisation resemble the usual macrodasyidan plan; however, the somatic circular muscles of the intestinal region surround all other muscular components and a third FMRFamide-IR commissure ventral to the pharyngo-intestinal junction appear to be an autoapomorphic traits of the new species.Conclusions/significanceWhile the anatomical characteristics of the Asian specimens appear so unique to grant the establishment of a new taxon, for which the name Thaidasys tongiorgii gen. et sp. nov. is proposed, the result of phylogenetic analyses based on the 18S rRNA gene unites the new genus with the family Macrodasyidae.

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Integrative taxonomy of a new Redudasys species (Gastrotricha: Macrodasyida) sheds light on the invasion of fresh water habitats by macrodasyids.

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