Dataset Information

Diversity and environmental distribution of the cosmopolitan endosymbiont "Candidatus Megaira".

ABSTRACT: Members of the order Rickettsiales are often found in association with ciliated protists. An interesting case is the bacterial endosymbiont "Candidatus Megaira", which is phylogenetically closely related to the pathogen Rickettsia. "Candidatus Megaira" was first described as an intracellular bacterium in several ciliate species. Since then it has been found in association with diverse evolutionary distantly-related hosts, among them other unicellular eukaryotes, and also algae, and metazoa, such as cnidarians. We provide the characterization of several new strains of the type species "Candidatus Megaira polyxenophila", and the multidisciplinary description of a novel species, "Candidatus Megaira venefica", presenting peculiar features, which highlight the diversity and variability of these widespread bacterial endosymbionts. Screening of the 16S rRNA gene short amplicon database and phylogenetic analysis of 16S rRNA gene hypervariable regions revealed the presence of further hidden lineages, and provided hints on the possibility that these bacteria may be horizontally transmitted among aquatic protists and metazoa. The phylogenetic reconstruction supports the existence of at least five different separate species-level clades of "Candidatus Megaira", and we designed a set of specific probes allowing easy recognition of the four major clades of the genus.

SUBMITTER: Lanzoni O

PROVIDER: S-EPMC6362216 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Diversity and environmental distribution of the cosmopolitan endosymbiont "Candidatus Megaira".

Lanzoni Olivia O Sabaneyeva Elena E Modeo Letizia L Castelli Michele M Lebedeva Natalia N Verni Franco F Schrallhammer Martina M Potekhin Alexey A Petroni Giulio G

Scientific reports 20190204 1

Members of the order Rickettsiales are often found in association with ciliated protists. An interesting case is the bacterial endosymbiont "Candidatus Megaira", which is phylogenetically closely related to the pathogen Rickettsia. "Candidatus Megaira" was first described as an intracellular bacterium in several ciliate species. Since then it has been found in association with diverse evolutionary distantly-related hosts, among them other unicellular eukaryotes, and also algae, and metazoa, such ...[more]

PMID: 30718604

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Project description:"Candidatus Megaira polyxenophila" is a recently described member of Rickettsiaceae which comprises exclusively obligate intracellular bacteria. Interestingly, these bacteria can be found in a huge diversity of eukaryotic hosts (protist, green algae, metazoa) living in marine, brackish or freshwater habitats. Screening of amplicon datasets revealed a high frequency of these bacteria especially in freshwater environments, most likely associated to eukaryotic hosts. The relationship of "Ca. Megaira polyxenophila" with their hosts and their impact on host fitness have not been studied so far. Even less is known regarding the responses of these intracellular bacteria to potential stressors. In this study, we used two phylogenetically close species of the freshwater ciliate Paramecium, Paramecium primaurelia and Paramecium pentaurelia (Ciliophora, Oligohymenophorea) naturally infected by "Ca. Megaira polyxenophila". In order to analyze the effect of the symbiont on the fitness of these two species, we compared the growth performance of both infected and aposymbiotic paramecia at different salinity levels in the range of freshwater and oligohaline brackish water i.e., at 0, 2, and 4.5 ppt. For the elimination of "Ca. Megaira polyxenophila" we established an antibiotic treatment to obtain symbiont-free lines and confirmed its success by fluorescence in situ hybridization (FISH). The population and infection dynamics during the growth experiment were observed by cell density counts and FISH. Paramecia fitness was compared applying generalized additive mixed models. Surprisingly, both infected Paramecium species showed higher densities under all salinity concentrations. The tested salinity concentrations did not significantly affect the growth of any of the two species directly, but we observed the loss of the endosymbiont after prolonged exposure to higher salinity levels. This experimental data might explain the higher frequency of "Ca. M. polyxenophila" in freshwater habitats as observed from amplicon data.

Project description:"Candidatus Accumulibacter" was the first microorganism identified as a polyphosphate-accumulating organism (PAO) important for phosphorus removal from wastewater. Members of this genus are diverse, and the current phylogeny and taxonomic framework appear complicated, with most publicly available genomes classified as "Candidatus Accumulibacter phosphatis," despite notable phylogenetic divergence. The ppk1 marker gene allows for a finer-scale differentiation into different "types" and "clades"; nevertheless, taxonomic assignments remain inconsistent across studies. Therefore, a comprehensive reevaluation is needed to establish a common understanding of this genus, in terms of both naming and basic conserved physiological traits. Here, we provide this reassessment using a comparison of genome, ppk1, and 16S rRNA gene-based approaches from comprehensive data sets. We identified 15 novel species, along with "Candidatus Accumulibacter phosphatis," "Candidatus Accumulibacter delftensis," and "Candidatus Accumulibacter aalborgensis." To compare the species in situ, we designed new species-specific fluorescence in situ hybridization (FISH) probes and revealed their morphology and arrangement in activated sludge. Based on the MiDAS global survey, "Ca. Accumulibacter" species were widespread in wastewater treatment plants (WWTPs) with phosphorus removal, indicating process design as a major driver for their abundance. Genome mining for PAO-related pathways and FISH-Raman microspectroscopy confirmed the potential for PAO metabolism in all "Ca. Accumulibacter" species, with detection in situ of the typical PAO storage polymers. Genome annotation further revealed differences in the nitrate/nitrite reduction pathways. This provides insights into the niche differentiation of these lineages, potentially explaining their coexistence in the same ecosystem while contributing to overall phosphorus and nitrogen removal. IMPORTANCE "Candidatus Accumulibacter" is the most studied PAO, with a primary role in biological nutrient removal. However, the species-level taxonomy of this lineage is convoluted due to the use of different phylogenetic markers or genome sequencing approaches. Here, we redefined the phylogeny of these organisms, proposing a comprehensive approach which could be used to address the classification of other diverse and uncultivated lineages. Using genome-resolved phylogeny, compared to phylogeny based on the 16S rRNA gene and other phylogenetic markers, we obtained a higher-resolution taxonomy and established a common understanding of this genus. Furthermore, genome mining of genes and pathways of interest, validated in situ by application of a new set of FISH probes and Raman microspectroscopy, provided additional high-resolution metabolic insights into these organisms.

Dataset Information

Diversity and environmental distribution of the cosmopolitan endosymbiont "Candidatus Megaira".

Publications

Diversity and environmental distribution of the cosmopolitan endosymbiont "Candidatus Megaira".

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