This study set out to bolster morphological and molecular datasets of marine gregarine apicomplexans. Gregarines were sampled from the Sea of Japan and Northwest Pacific from cirratuliform ...polychaetes (Acrocirridae, Cirratulidae, and Flabelligeridae), as well as sipunculids. Trophozoites (feeding stages) were gathered for identification using light microscopy, scanning electron microscopy, and transmission electron microscopy. Cells were also collected for molecular phylogenetic analysis using 18S rDNA and 28S rDNA. As a result, three new species of Selenidium, S. planusae n. sp., S. validusae n. sp., and S. pyroidea n. sp. were described, and additional morphological and genetic data were gathered for an existing species, S. orientale; and Trollidium was established as a new genus. Trollidium akkeshiense n. gen. n. sp. possessed a unique, unsymmetrical organization of microtubules running the longitudinal length of one side of the trophozoite, corresponding to a zig-zag pattern of epicytic (surface) folds, and a flicking pattern of movement. Phylogenetic analyses of 18S rDNA and 28S rDNA showed that these portions of the ribosomal operon are able to resolve some relationships among Selenidium, while other lineages including Trollidium akkeshiense n. gen. n. sp. appeared to be highly influenced by long branch attraction. High evolutionary rates along the ribosomal operon of gregarines may hinder this marker from resolving deeper nodes among early apicomplexans.
Gregarines are an early-diverging lineage of apicomplexan parasites that hold many clues into the origin and evolution of the group, a remarkable transition from free-living phototrophic algae into ...obligate parasites of animals.1 Using single-cell transcriptomics targeting understudied lineages to complement available sequencing data, we characterized the mitochondrial metabolic repertoire across the tree of apicomplexans. In contrast to the large suite of proteins involved in aerobic respiration in well-studied parasites like Toxoplasma or Plasmodium,2 we find that gregarine trophozoites have significantly reduced energy metabolism: most lack respiratory complexes III and IV, and some lack the electron transport chains (ETCs) and tricarboxylic acid (TCA) cycle entirely. Phylogenomic analyses show that these reductions took place several times in parallel, resulting in a functional range from fully aerobic organelles to extremely reduced “mitosomes” restricted to Fe-S cluster biosynthesis. The mitochondrial genome has also been lost repeatedly: in species with severe functional reduction simply by gene loss but in one species with a complete ETC by relocating cox1 to the nuclear genome. Severe functional reduction of mitochondria is generally associated with structural reduction, resulting in small, nondescript mitochondrial-related organelles (MROs).3 By contrast, gregarines retain distinctive mitochondria with tubular cristae, even the most functionally reduced cases that also lack genes associated with cristae formation. Overall, the parallel, severe reduction of gregarine mitochondria expands the diversity of organisms that contain MROs and further emphasizes the role of parallel transitions in apicomplexan evolution.
•Single-cell transcriptomics of diverse apicomplexan parasites of invertebrates•Reconstruction of the mitochondrial metabolic repertoire across apicomplexans•Discovery of a range of reduced mitochondrion-related organelles in gregarines•Multiple, parallel losses of electron transport and aerobic energy metabolism
Mathur et al. show that gregarine apicomplexans have significantly reduced mitochondria: most lack complexes III and IV, and some lack the respiratory chain and TCA cycle entirely. Phylogenomics show that these reductions took place many times in parallel, resulting in a functional range from fully aerobic mitochondria to highly reduced mitosomes.
Abstract
Motivation
Motivated by the challenges of decentralized genetic data spread across multiple international organizations, GINSA leverages the Global Biodiversity Information Facility ...infrastructure to automatically retrieve and link small ribosomal subunit sequences with locality information.
Results
Testing on taxa from major organism groups demonstrates broad applicability across taxonomic levels and dataset sizes.
Availability and implementation
GINSA is a freely accessible Python program under the MIT License and can be installed from PyPI via pip.
Acoels in the family Convolutidae are commonly found with microalgal symbionts. Convolutids can host green algal
Tetraselmis
and dinoflagellates within the family Symbiodiniaceae and the genus
...Amphidinium
. The diversity of these microalgae has not been well surveyed. In this study, we used PCR and culture techniques to demonstrate the biodiversity of
Tetraselmis
and dinoflagellates in symbiosis with meiofaunal acoels. Here, 66 acoels were collected from seven localities around Okinawa, Ishigaki, and Kochi, Japan. While convolutids were heavily represented in this sampling, some acoels formed a clade outside Convolutidae and are potentially a new family of acoels harboring symbiotic microalgae. From the acoels collected, a total of 32
Tetraselmis
and 26 Symbiodiniaceae cultures were established. Molecular phylogenies were constructed from cultured material (and from total host DNA) using the 18S rRNA gene (
Tetraselmis
) and 28S rRNA gene (dinoflagellates). The majority of
Tetraselmis
sequences grouped within the
T
.
astigmatica
clade but strains closely related to
T
.
convolutae
,
T
.
marina
, and
T
.
gracilis
were also observed. This is the first report of
Tetraselmis
species, other than
T
.
convolutae
, naturally associating with acoels. For dinoflagellates, members of
Cladocopium
and
Miliolidium
were observed, but most Symbiodiniaceae sequences formed clusters within
Symbiodinium
, grouping with
S
.
natans
, or sister to
S
.
tridacnidorum
. Several new
Symbiodinium
sequences from this study may represent novel species. This is the first molecular record of
Miliolidium
and
Symbiodinium
from acoels. Microalgal strains from this study will provide a necessary framework for future taxonomic studies and research on symbiotic relationships between acoels and microalgae.
Summary
The application of metabarcoding to study animal‐associated microeukaryotes has been restricted because the universal barcode used to study microeukaryotic ecology and distribution in the ...environment, the Small Subunit of the Ribosomal RNA gene (18S rRNA), is also present in the host. As a result, when host‐associated microbial eukaryotes are analysed by metabarcoding, the reads tend to be dominated by host sequences. We have done an in silico validation against the SILVA 18S rRNA database of a non‐metazoan primer set (primers that are biased against the metazoan 18S rRNA) that recovers only 2.6% of all the metazoan sequences, while recovering most of the other eukaryotes (80.4%). Among metazoans, the non‐metazoan primers are predicted to amplify 74% of Porifera sequences, 4% of Ctenophora, and 15% of Cnidaria, while amplifying almost no sequences within Bilateria. In vivo, these non‐metazoan primers reduce significantly the animal signal from coral and human samples, and when compared against universal primers provide at worst a 2‐fold decrease in the number of metazoan reads and at best a 2800‐fold decrease. This easy, inexpensive, and near‐universal method for the study of animal‐associated microeukaryotes diversity will contribute to a better understanding of the microbiome.
Coral geometry and why it matters Kahng, Samuel E; Odle, Eric; Wakeman, Kevin C
PeerJ (San Francisco, CA),
02/2024, Letnik:
12
Journal Article
Recenzirano
Odprti dostop
Clonal organisms like reef building corals exhibit a wide variety of colony morphologies and geometric shapes which can have many physiological and ecological implications. Colony geometry can ...dictate the relationship between dimensions of volume, surface area, and length, and their associated growth parameters. For calcifying organisms, there is the added dimension of two distinct components of growth, biomass production and calcification. For reef building coral, basic geometric shapes can be used to model the inherent mathematical relationships between various growth parameters and how colony geometry determines which relationships are size-dependent or size-independent. Coral linear extension rates have traditionally been assumed to be size-independent. However, even with a constant calcification rate, extension rates can vary as a function of colony size by virtue of its geometry. Whether the ratio between mass and surface area remains constant or changes with colony size is the determining factor. For some geometric shapes, the coupling of biomass production (proportional to surface area productivity) and calcification (proportional to volume) can cause one aspect of growth to geometrically constrain the other. The nature of this relationship contributes to a species' life history strategy and has important ecological implications. At one extreme, thin diameter branching corals can maximize growth in surface area and resource acquisition potential, but this geometry requires high biomass production to cover the fast growth in surface area. At the other extreme, growth in large, hemispheroidal corals can be constrained by calcification. These corals grow surface area relatively slowly, thereby retaining a surplus capacity for biomass production which can be allocated towards other anabolic processes. For hemispheroidal corals, the rate of surface area growth rapidly decreases as colony size increases. This ontogenetic relationship underlies the success of microfragmentation used to accelerate restoration of coral cover. However, ontogenetic changes in surface area productivity only applies to certain coral geometries where surface area to volume ratios decrease with colony size.
Microturbellarians are abundant and ubiquitous members of marine meiofaunal communities around the world. Because of their small body size, these microscopic animals are rarely considered as hosts ...for parasitic organisms. Indeed, many protists, both free-living and parasitic ones, equal or surpass meiofaunal animals in size. Despite several anecdotal records of "gregarines", "sporozoans", and "apicomplexans" parasitizing microturbellarians in the literature-some of them dating back to the nineteenth century-these single-celled parasites have never been identified and characterized. More recently, the sequencing of eukaryotic microbiomes in microscopic invertebrates have revealed a hidden diversity of protist parasites infecting microturbellarians and other meiofaunal animals. Here we show that apicomplexans isolated from twelve taxonomically diverse rhabdocoel taxa and one species of proseriate collected in four geographically distinct areas around the Pacific Ocean (Okinawa, Hokkaido, and British Columbia) and the Caribbean Sea (Curaçao) all belong to the apicomplexan genus Rhytidocystis. Based on comprehensive molecular phylogenies of Rhabdocoela and Proseriata inferred from both 18S and 28S rDNA sequences, as well as a molecular phylogeny of Marosporida inferred from 18S rDNA sequences, we determine the phylogenetic positions of the microturbellarian hosts and their parasites. Multiple lines of evidence, including morphological and molecular data, show that at least nine new species of Rhytidocystis infect the microturbellarian hosts collected in this study, more than doubling the number of previously recognized species of Rhytidocystis, all of which infect polychaete hosts. A cophylogenetic analysis examining patterns of phylosymbiosis between hosts and parasites suggests a complex picture of overall incongruence between host and parasite phylogenies, and varying degrees of geographic signals and taxon specificity.
Gregarines are the most biodiverse group of apicomplexan parasites. This group specializes on invertebrate hosts (e.g., ascidians, crustaceans, and polychaetes). Marine gregarines are of particular ...interest because they are considered to be the earliest evolving apicomplexan lineage, having subsequently speciated (and radiated) through virtually all existing animal groups. Still, mechanisms governing the broad (global) distribution and speciation patterns of apicomplexans are not well understood. The present study examines Pacific lecudinids, one of the most species-rich and diverse groups of marine gregarines. Here, marine polychaetes were collected from intertidal zones. Single trophozoite cells were isolated for light and electron microscopy, as well as molecular phylogenetic analyses using the partial 18S rRNA gene. The cytochrome c oxidase subunit 1 gene was used to confirm morphology-based host identification. This study introduces Undularius glycerae n. gen., n. sp. and Lecudina kitase n. sp. (Hokkaido, Japan), as well as Difficilina fasoliformis n. sp. (California, USA). Occurrences of Lecudina cf. longissima and Lecudina cf. tuzetae (California, USA) are also reported. Phylogenetic analysis revealed a close relationship between L. pellucida, L. tuzetae, and L. kitase n. sp. Additionally, clustering among North Atlantic and Pacific L. tuzetae formed a species complex, likely influenced by biogeography.
Platyproteum is an enigmatic, monotypic genus formerly assigned to the Apicomplexa, until a recent phylogenomic study demonstrated that it diverged from the base of the chromerid/colpodellid ...(chrompodellid) taxa and apicomplexan clade. In the present study, a new species, P. noduliferae n. sp., is described using a combination of morphological and molecular data. Moreover, a reconstruction of the flagellar apparatus is presented to characterize the presence of flagella which was, until this study, an unknown trait for this genus. Phylogenetic analyses using rDNA sequences suggested that P. noduliferae n. sp. is a sister species of P. vivax, diverging from the base of chrompodellids and apicomplexans. This study provides new morphological data that corroborates the position of Platyproteum amongst other biflagellate species, contributing to an improved understanding of Platyproteum and the evolutionary changes undergone by some marine alveolates as they transitioned into obligate parasitic life styles.
Marine benthic dinoflagellates within the genus Amphidinium were isolated from Guam and Okinawa. Isolated strains were identified to species-level using phylogenetic analyses of 28S rRNA and ITS-5.8S ...rRNA genes as well as microscopy. Of the six isolated strains, two were new species: A. pagoense sp. nov. and A. uduigamense sp. nov. Other isolates included strains of A. massartii and A. operculatum from Guam, and two strains of A. operculatum from Okinawa. Both new species were described using light and electron microscopy (SEM and TEM). The combination of characteristics that make A. pagoense sp. nov. unique includes a pair of centrally-located pyrenoids, variable cell shape, absence of scales and a long, curved ventral ridge. For A. uduigamense sp. nov., a combination of several morphological features distinguishes it from other species. These include a constriction near the anterior of the hypocone, two centrally located pyrenoids, a longitudinal flagellum inserted in the posterior one-third of the cell, cell size, cell division in the motile stage and the absence of scales. Toxicity was confirmed in these two novel species by testing methanol extracts in an Artemia bioassay. Previously unrecorded ITS rRNA gene sequences from A. operculatum were also sequenced from both locations. Species identified and newly described in this study expand the taxonomic knowledge of Amphidinium in the Pacific.
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