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Petroni, G.

Publications and source records attributed to Petroni, G..

9 recordsLinked to original sources

Environmental DNA reveals long-term persistence of a Midichloria-like bacterium in a rainbow trout aquaculture and links Ichthyopthirius multifiliis with the red mark syndrome

Red Mark Syndrome (RMS) is a widespread skin disease affecting rainbow trout (Onchorhynchus mykiss). It provokes substantial economic losses in aquaculture, and is putatively caused by a Rickettsiales bacterium named Midichloria-like organism (RMS-MLO), which is strongly associated with RMS lesions. However, RMS-MLO ecology and epidemiology in aquaculture systems remain poorly understood. In this study, we analysed environmental DNA to monitor the presence of RMS-MLO and its putative vector Ichthyophthirius multifiliis in a trout farm in Northern Italy over one year. Water and sediment samples were monthly collected from multiple water tanks. RMS-MLO was consistently detected by PCR throughout the study in all trout-containing tanks, both in water and sediment samples, but never in the trout-free inflow tank. We did not observe an increase in RMS-MLO abundance during the single RMS outbreak recorded nor in relation with the co-occurrence of I. multifiliis. Our findings indicate a long-term persistence of RMS-MLO in the aquaculture, possibly as a consequence of infections with low prevalence or abundance, rather than its entry from the external environment at the time of RMS outbreaks. Additionally, hints were recorded for a potential role of free-living aquatic microeukaryotes as additional occasional reservoirs. In contrast, I. multifiliis was negatively related with RMS-MLO, while it significantly increased in abundance during the RMS outbreak, particularly in the inflow tank. This supports that, rather than a stable reservoir, I. multifiliis may act as a facilitator of RMS outbreaks, which might indeed be triggered by the entry of this parasite in trout farms.

microbiology↗

Evolution at experimental epidemic fronts speeds up parasite spread

Spreading epidemics can foster the rapid emergence of novel parasite variants. Similar to range expansions, parasites at the front of an epidemic wave may evolve traits facilitating their spatial spread. Typically, higher transmissibility and virulence are expected to evolve at the epidemic front, but predictions change if virulence reduces dispersal of infected hosts. We investigated the feedbacks between epidemiology and evolution in interconnected microcosms of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata. First, two long-term treatments mimicked the moving front of epidemic waves, with and without the natural dispersal of infected hosts. Phenotypic trait assays revealed an eco-to-evo feedback: front parasites (i.e., travelling with infected hosts) were less virulent and interfered less with host dispersal, but also showed higher infectivity, compared to parasites from the control treatment. Whole-genome resequencing and analyses of functional genomic diversity corroborated such phenotypic divergence. Second, measurement of the spread of evolved parasites in linear landscapes demonstrated an evo-to-eco feedback: front parasites produced stronger infection outbreaks and faster spreading epidemic waves than did control parasites. A simulation model assessed the relative importance of the different parasite traits in determining infectious spread over a broad parameter range. It suggests that, if dispersal is generally low, higher infectivity alone can produce the observed differences in epidemic spread speed. Our study illustrates how the need to travel with the host shapes eco-evolutionary feedbacks at parasite invasion fronts, and it highlights the importance of considering concomitant evolutionary change when predicting epidemic speed. Significance StatementWhen predicting disease spread across spatial scales it is fundamental to consider host dispersal, but also the concomitant evolution of parasite traits such as infectivity and virulence. We tested how dispersal constraints affect parasite evolution and epidemic spread in an aquatic model system, by combining experimental evolution, genetic analysis and mathematical modelling. Our results suggest that epidemics can be accelerated by the evolution of highly infectious, but not necessarily more virulent parasites, in contrast to conventional views. This illustrates the important role of eco-evolutionary feedback loops can play in shaping the spread of emerging or geographically expanding parasites.

evolutionary biology↗

Description of three new predator species of Litostomatea (Alveolata, Ciliophora), including sequencing and annotation of their mitochondrial genomes

Three new species of haptorian ciliates Lacrymaria venatrix sp. nov., Phialina famelica sp. nov., and Chanaea vermicularis sp. nov., recovered from water bodies of Tuscany, Italy, are described according to the standards of the Next Generation Taxonomy, which include morphology, ultrastructure, phylogeny, and associated microbial consortium analysis plus mitochondrial genome sequencing and annotation. Lacrymaria venatrix is a species with a small spindle-shaped trunk, a highly contractile neck that equals the trunk in length at its full extension, and a macronucleus consisting of two nodules; it is mostly similar to L. songi but diverges in the denser ciliature, the closer macronuclear nodules, and the single micronucleus. Phialina famelica has a blunter spindle-shaped trunk with a shallow oral bulge and an elongated macronucleus; it is mostly similar to P. salinarum and P. serranoi, but differs in the freshwater habitat, and by having fewer but denser kineties. Chaenea vermicularis differs from its congenerics by a modest contractility combined with a greater elongation ability, the mucocysts organized into multiple rows forming stripes, and the several hundreds of macronuclear nodules. The 18S rDNA-based phylogenetic analysis supports previous observations of the paraphyly of the genera Lacrymaria and Phialina, that need a deep systematics revision. The genus Chaenea seems not to be challenged, though its position within Haptoria remains not fully clear, and C. vermicularis sp. nov. appears rather divergent from its congeners.

zoology↗

Macroinvertebrate diversity patterns in a guano-rich temperate cave

Most caves in temperate regions are energy-poor, leading to low richness and abundances of terrestrial macroinvertebrates. However, caves with abundant bat populations may represent a notable exception, as bat guano serves as a significant source of organic matter, supporting diverse specialized invertebrates. Yet, given the overall rarity of guano-rich caves in temperate region, their ecological dynamics are poorly understood. We conducted a year-long monthly standardized monitoring of the macroinvertebrates of the Buca dei Ladri cave, a guano-rich cavity in Tuscany, Italy. At each survey, we counted species within different sampling quadrats and collected environmental variables such as temperature, structural heterogeneity of the substrate, dominant substrate, and presence of bats. Over the year, we identified 31 macroinvertebrate species in the cave as both morphospecies and molecular lineages, based on mitochondrial COI and nuclear 18S genes. The latter approach hinted at the presence of cryptic diversity in some species. We observed an increase in species diversity with increasing structural complexity and the presence of bats, whereas a lower species diversity was found in guano-dominated substrates, probably due to the old age and subsequent low nutritional value of the historical guano deposits. Changes in the abundance of species within the cave were primarily explained by differences in structural complexity across sampling quadrats, whereas the distance from the cave entrance mostly explained species replacement. Our results underscore the importance of preserving healthy bat populations and a high habitat heterogeneity within the cave for the long-term conservation of the unique macroinvertebrate assemblages of the cave.

ecology↗

Host association and intracellularity evolved multiple times independently in the Rickettsiales

The order Rickettsiales (Alphaproteobacteria) encompasses multiple diverse lineages of host-associated bacteria, including pathogens, reproductive manipulators, and mutualists. In order to understand how intracellularity and host association originated in this order, and whether they are ancestral or convergently evolved characteristics, we built an unprecedentedly large and phylogenetically-balanced dataset that includes de novo sequenced genomes and an accurate selection of published genomic and metagenomic assemblies. We performed detailed functional reconstructions that clearly indicated "late" and parallel evolution of obligate host-association and intracellularity in different Rickettsiales lineages. According to the depicted scenario, multiple independent series of horizontal acquisitions of transporters led to the progressive loss of biosynthesis of nucleotides, amino acids and other metabolites, producing distinct conditions of host-dependence. Coherently, each clade experienced a different pattern of evolution of the ancestral arsenal of interaction apparatuses, including development of specialised effectors involved in the lineage-specific mechanisms of host cell adhesion/invasion and intracellularity.

microbiology↗

Ciliated protozoa from industrial WWTP activated sludge: a biodiversity survey including trophic interactions and redescription of Bakuella subtropica (Spirotrichea, Hypotrichia) according to Next Generation Taxonomy

Optimization of wastewater treatment with biological processes is a fundamental challenge of modern society. During past years new technologies have been developed for the purpose and prokaryotic organisms involved in the process extensively investigated. Nevertheless, relatively few studies so far analysed the protozoan community in these systems using modern integrative approaches, despite its obvious role in shaping ecological dynamics and, possibly, process efficiency. In the present study, we characterized the ciliate community in biological reactors of an Italian industrial (tannery) wastewater treatment plant (WWTP) applying modified Ludzack-Ettinger (MLE) process. This plant is characterized by moderate salinity, high solids retention time and high concentration of organic compounds, including a significant recalcitrant fraction. We performed the morphological and 18S rDNA characterizations of almost all the 21 ciliates retrieved along a one-year sampling period, and provided preliminary data on species occurrence, community dynamics, and trophic interactions. Only 16 species were observed on the sample collection day and most of them had an occurrence higher than 50%. The most frequently occurring and highly abundant organisms were Aspidisca cf. cicada, Euplotes spp., Paramecium calkinsi, and Phialina sp. Cyclidium cf. marinum was only found on a single date and its presence was possibly related to a summer break-induced perturbation. All the species showed the capability to survive the short oxic/anoxic cycling typical of the studied WWTP process. Intriguingly, some of them (i.e., Bakuella subtropica and Trochiliopsis australis) turned out to be species isolated from brackish natural environment rich in organic load as well. As for B. subtropica, we provided an emended redescription according to the most recent taxonomy standards that include also mitogenomic sequencing.

zoology↗

Outwitting planarians antibacterial defence mechanisms: Rickettsiales bacterial trans-infection from Paramecium multimicronucleatum to planarians

Most of the microorganisms belonging to genera responsible for vector-borne diseases (VBD) have hematophagous arthropods as vector/reservoir. Recently, many new species of microorganisms phylogenetically related to agents of VBD were found in a variety of aquatic eukaryotic hosts, in particular, numerous new bacterial species related to the genus Rickettsia (Alphaproteobacteria, Rickettsiales) were discovered in protist ciliates and other unicellular eukaryotes. Although their pathogenicity for humans and terrestrial animals is not known, these bacteria might act as etiological agents of possible VBD of aquatic organisms, with protist as vectors. In the present study, we characterized a novel strain of the Rickettsia-Like Organism (RLO) endosymbiont \"Candidatus (Ca.) Trichorickettsia mobilis\" in the macronucleus of the ciliate Paramecium multimicronucleatum through Fluorescence In Situ Hybridization (FISH) and molecular analyses. Ultrastructural investigations on the presence of flagella confirmed previous studies on the same bacterial species. The potential trans-infection per os of this bacterium to planarians (Dugesia japonica), a widely used model system able to eliminate a wide range of bacteria pathogenic to humans and other Metazoa, was further verified. Ciliate mass cultures were set up, and trans-infection experiments were performed by adding homogenized paramecia to food of antibiotic-treated planarians, performed. Treated and non-treated (i.e. control) planarians were investigated at day 1, 3, and 7 after feeding for endosymbiont presence by means of PCR and ultrastructural analyses. Obtained results were fully concordant and suggest that this RLO endosymbiont can be transferred from ciliates to metazoans, being detected up to day 7 in treated planarian enterocytes inside and, possibly, outside phagosomes.

microbiology↗

Next generation taxonomy: integrating traditional species description with the holobiont concept and genomic approaches - The in-depth characterization of a novel Euplotes species as a case study

In 1991 Margulis defined holobionts as the assemblage of \"two or more organisms, members of different species\" which remain associate \"throughout a significant portion of the life history\". In recent times, holobionts have been described among many and far-related groups of living beings, such as plants, algae, insects, corals, and even humans. These studies have arisen an increasing interest in different contexts but, to our knowledge, the holobiont concept has not been applied in taxonomy. Here we propose a new approach to modern taxonomy, aimed to integrate the holobiont concept and genomic and bioinformatic analyses with the classical/morphological tools traditionally used in taxonomy. The inclusion of symbiont morphology, and of mitochondrial and symbiont genomes will allow the discipline to move toward what could become the \"next generation taxonomy\". As an example of this new paradigm in the characterization of holobionts, we herein provide the taxonomic description of the ciliate protist Euplotes vanleeuwenhoeki sp. nov. (Euplotia, Ciliophora) and its bacterial endosymbiont \"Candidatus Pinguicoccus supinus\" gen. nov., sp. nov. (Opitutae, Verrucomicrobia). Interestingly, we found that this endosymbiont has an extremely reduced genome (~163 Kbp), which is suggestive of a high integration with the host and represents the first case of such an extreme reduction in Verrucomicrobia, and the first case in a protist host.

zoology↗

The extracellular association of the bacterium \"Candidatus Deianiraea vastatrix\" with the ciliate Paramecium suggests an alternative scenario for the evolution of Rickettsiales

Rickettsiales are a lineage of obligatorily intracellular Alphaproteobacteria, encompassing important human pathogens, manipulators of host reproduction, and mutualists. Here we report the discovery of a novel Rickettsiales bacterium associated with Paramecium, displaying a unique extracellular lifestyle, including the ability to replicate outside host cells. Genomic analyses show that the bacterium possesses a higher capability to synthesize amino acids, compared to all investigated Rickettsiales. Considering these observations, phylogenetic and phylogenomic reconstructions, and re-evaluating the different means of interaction of Rickettsiales bacteria with eukaryotic cells, we propose an alternative scenario for the evolution of intracellularity in Rickettsiales. According to our reconstruction, the Rickettsiales ancestor would have been an extracellular and metabolically versatile bacterium, while obligate intracellularity and genome reduction would have evolved later in parallel and independently in different sub-lineages. The proposed new scenario could impact on the open debate on the lifestyle of the last common ancestor of mitochondria within Alphaproteobacteria.

evolutionary biology↗