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Giulio Petroni - One of the best experts on this subject based on the ideXlab platform.
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candidatus sarmatiella mevalonica endosymbiont of the ciliate paramecium provides insights on evolutionary plasticity among Rickettsiales
Environmental Microbiology, 2021Co-Authors: Michele Castelli, Letizia Modeo, Olivia Lanzoni, Alexey Potekhin, Davide Sassera, Tiago Nardi, Stefano Lometto, Giulio PetroniAbstract:Members of the bacterial order Rickettsiales are obligatorily associated with a wide range of eukaryotic hosts. Their evolutionary trajectories, in particular concerning the origin of shared or differential traits among distant sub-lineages, are still poorly understood. Here we characterised a novel Rickettsiales bacterium associated with the ciliate Paramecium tredecaurelia, and phylogenetically related to the Rickettsia genus. Its genome encodes significant lineage-specific features, chiefly the mevalonate pathway gene repertoire, involved in isoprenoid precursor biosynthesis. Not only this pathway has never been described in Rickettsiales, it also is very rare among bacteria, though typical in eukaryotes, thus likely representing a horizontally-acquired trait. The presence of these genes could enable an efficient exploitation of host-derived intermediates for isoprenoid synthesis. Moreover, we hypothesise the reversed reactions could have replaced canonical pathways for producing acetyl-CoA, essential for phospholipid biosynthesis. Additionally, we detected phylogenetically unrelated mevalonate pathway genes in metagenome-derived Rickettsiales sequences, likely indicating evolutionary convergent effects of independent horizontal gene transfer events. Accordingly, convergence, involving both gene acquisitions and losses, is highlighted as a relevant evolutionary phenomenon in Rickettsiales, possibly favoured by plasticity and comparable lifestyles, representing a potentially hidden origin of other more nuanced similarities among sub-lineages. This article is protected by copyright. All rights reserved.
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the genome sequence of candidatus fokinia solitaria insights on reductive evolution in Rickettsiales
Genome Biology and Evolution, 2018Co-Authors: Anna Maria Floriano, Giulio Petroni, Michele Castelli, Sascha Krenek, Thomas U Berendonk, C Bazzocchi, Davide SasseraAbstract:"Candidatus Fokinia solitaria" is an obligate intracellular endosymbiont of a unicellular eukaryote, a ciliate of the genus Paramecium. Here, we present the genome sequence of this bacterium and subsequent analysis. Phylogenomic analysis confirmed the previously reported positioning of the symbiont within the "Candidatus Midichloriaceae" family (order Rickettsiales), as well as its high sequence divergence from other members of the family, indicative of fast sequence evolution. Consistently with this high evolutionary rate, a comparative genomic analysis revealed that the genome of this symbiont is the smallest of the Rickettsiales to date. The reduced genome does not present flagellar genes, nor the pathway for the biosynthesis of lipopolysaccharides (present in all the other so far sequenced members of the family "Candidatus Midichloriaceae") or genes for the Krebs cycle (present, although not always complete, in Rickettsiales). These results indicate an evolutionary trend toward a stronger dependence on the host, in comparison with other members of the family. Two alternative scenarios are compatible with our results; "Candidatus Fokinia solitaria" could be either a recently evolved, vertically transmitted mutualist, or a parasite with a high host-specificity.
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disentangling the taxonomy of Rickettsiales and description of two novel symbionts candidatus bealeia paramacronuclearis and candidatus fokinia cryptica sharing the cytoplasm of the ciliate protist paramecium biaurelia
Applied and Environmental Microbiology, 2016Co-Authors: Michele Castelli, Elena Sabaneyeva, Franziska Szokoli, Martina Schrallhammer, Sascha Krenek, Thomas G Doak, Thomas U Berendonk, Giulio PetroniAbstract:ABSTRACT In the past 10 years, the number of endosymbionts described within the bacterial order Rickettsiales has constantly grown. Since 2006, 18 novel Rickettsiales genera inhabiting protists, such as ciliates and amoebae, have been described. In this work, we characterize two novel bacterial endosymbionts from Paramecium collected near Bloomington, IN. Both endosymbiotic species inhabit the cytoplasm of the same host. The Gram-negative bacterium “Candidatus Bealeia paramacronuclearis” occurs in clumps and is frequently associated with the host macronucleus. With its electron-dense cytoplasm and a distinct halo surrounding the cell, it is easily distinguishable from the second smaller symbiont, “Candidatus Fokinia cryptica,” whose cytoplasm is electron lucid, lacks a halo, and is always surrounded by a symbiontophorous vacuole. For molecular characterization, the small-subunit rRNA genes were sequenced and used for taxonomic assignment as well as the design of species-specific oligonucleotide probes. Phylogenetic analyses revealed that “Candidatus Bealeia paramacronuclearis” clusters with the so-called “basal” Rickettsiales, and “Candidatus Fokinia cryptica” belongs to “Candidatus Midichloriaceae.” We obtained tree topologies showing a separation of Rickettsiales into at least two groups: one represented by the families Rickettsiaceae, Anaplasmataceae, and “Candidatus Midichloriaceae” (RAM clade), and the other represented by “basal Rickettsiales,” including “Candidatus Bealeia paramacronuclearis.” Therefore, and in accordance with recent publications, we propose to limit the order Rickettsiales to the RAM clade and to raise “basal Rickettsiales” to an independent order, Holosporales ord. nov., inside Alphaproteobacteria, which presently includes four family-level clades. Additionally, we define the family “Candidatus Hepatincolaceae” and redefine the family Holosporaceae. IMPORTANCE In this paper, we provide the characterization of two novel bacterial symbionts inhabiting the same Paramecium host (Ciliophora, Alveolata). Both symbionts belong to “traditional” Rickettsiales, one representing a new species of the genus “Candidatus Fokinia” (“Candidatus Midichloriaceae”), and the other representing a new genus of a “basal” Rickettsiales. According to newly characterized sequences and to a critical revision of recent literature, we propose a taxonomic reorganization of “traditional” Rickettsiales that we split into two orders: Rickettsiales sensu stricto and Holosporales ord. nov. This work represents a critical revision, including new records of a group of symbionts frequently occurring in protists and whose biodiversity is still largely underestimated.
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Protist ciliates as natural reservoir for bacteria potentially pathogenic for metazoan: preliminary results of the experimental infection of the planarian Dugesia.
2016Co-Authors: Letizia Modeo, Di Giuseppe Graziano, Alessandra Salvetti, Leonardo Rossi, Claudia Vannini, Sergey Fokin, Giulio Petroni, Franco VerniAbstract:Most of the microorganisms belonging to genera responsible for vector-borne diseases (VBD) has hematophagous arthropods as vector/reservoir. Recently, many new species of such microorganisms were found in a variety of terrestrial and aquatic eukaryotic hosts: in particular, numerous new bacterial species belonging/related to the genus Rickettsia, Alphaproteobacteria of the order Rickettsiales with an obligate intracellular lifestyle (e.g. the etiological agents of epidemic typhus and spotted fever), were discovered in protist ciliates. Although their pathogenicity for either humans or animals is still under study, these bacteria could actually act as etiological agents of possible VBD of aquatic environment. Indeed, an increasing number of massive fish death was recorded in intensive aquaculture facilities during the lasts years due to epidemics caused by Rickettsia-like bacteria with unknown natural vector. As ciliates could vector pathogenic organisms possibly responsible for zoonosis, we intended to verify the transmission of the Rickettsiales endosymbionts hosted by two species of ciliates to a metazoan model, the planarian Dugesia japonica. The ciliates were Euplotes woodruffi and Paramecium multimicronucleatum; the first hosts in the cytoplasm two different Rickettsiales endosymbionts, “Candidatus (Ca) Megaira polyxenophila” and “Ca. Bandiella woodruffii”, in addition to the betaproteobacterium Polynucleobacter necessarius; the second hosts in the macronucleus the Rickettsiales endosymbiont “Ca. Trichorickettsia mobilis”. Ciliate monoclonal mass cultures were set up to perform the following infection experiments: 1. Ciliate washing, concentrating, homogenizing, and addition to regular food for planarians. 2. Antibiotic-treated planarians feeding on ciliate-enriched food or regular food (as control), then washing and letting digest for 24, 48, and 72 h; 3. Comparative multidisciplinary investigation: molecular analyses, whole mount in situ hybridization, and TEM observation. Preliminary results are encouraging: we recovered endosymbionts up to 72 h after feeding, and identified them in planarians’ intestine and digestive vacuoles in TEM material. Endosymbionts were frequently observed near vacuole edge, with vacuole membrane sometimes somehow interrupted. TEM results were compared with literature data where endosymbionts were demonstrated to escape vacuoles invading the cytoplasm. Financial support: PRA 2016, University of Pisa
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biodiversity of non model Rickettsiales and their association with aquatic organisms
2016Co-Authors: Michele Castelli, Davide Sassera, Giulio PetroniAbstract:Representatives of the order Rickettsiales are obligate intracellular bacteria, traditionally including well-studied pathogens of humans and other vertebrates, such as Rickettsia, Orientia, Anaplasma, and Ehrlichia. In the last two decades, studies based on molecular characterization techniques have reshaped our view on the biodiversity of Rickettsiales, and the eukaryotic hosts they can exploit. Several new genera have been described in “traditional” Rickettsiales families Rickettsiaceae and Anaplasmataceae. Moreover, a new family, “Candidatus Midichloriaceae,” displaying diversity at least comparable with the “traditional” ones, has been described. Recent data show that the majority of extant genera of Rickettsiales (16 out of 24) are hosted exclusively (or at least partly) by aquatic organisms, such as protists (e.g., ciliates, amoebas, flagellates), and animals (e.g., cnidarians, mollusks, tunicates, leeches), while only ten genera include some terrestrial host, such as arthropods. Given the highly interwoven phylogenetic relationships among Rickettsiales hosted by aquatic and terrestrial hosts, it is likely that the ancestral host of Rickettsiales was an aquatic protist organism, and the adaptation to terrestrial environments occurred independently in several distinct sublineages at least six times. Newly discovered lineages of “non-model” Rickettsiales present unforeseen features for the order such as the presence of flagella. Future investigations on “non-model” Rickettsiales are crucial to gain insight on the evolutionary history of the whole group, including the origin of molecular mechanisms involved in pathogenesis for humans and vertebrates.
Michele Castelli - One of the best experts on this subject based on the ideXlab platform.
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candidatus sarmatiella mevalonica endosymbiont of the ciliate paramecium provides insights on evolutionary plasticity among Rickettsiales
Environmental Microbiology, 2021Co-Authors: Michele Castelli, Letizia Modeo, Olivia Lanzoni, Alexey Potekhin, Davide Sassera, Tiago Nardi, Stefano Lometto, Giulio PetroniAbstract:Members of the bacterial order Rickettsiales are obligatorily associated with a wide range of eukaryotic hosts. Their evolutionary trajectories, in particular concerning the origin of shared or differential traits among distant sub-lineages, are still poorly understood. Here we characterised a novel Rickettsiales bacterium associated with the ciliate Paramecium tredecaurelia, and phylogenetically related to the Rickettsia genus. Its genome encodes significant lineage-specific features, chiefly the mevalonate pathway gene repertoire, involved in isoprenoid precursor biosynthesis. Not only this pathway has never been described in Rickettsiales, it also is very rare among bacteria, though typical in eukaryotes, thus likely representing a horizontally-acquired trait. The presence of these genes could enable an efficient exploitation of host-derived intermediates for isoprenoid synthesis. Moreover, we hypothesise the reversed reactions could have replaced canonical pathways for producing acetyl-CoA, essential for phospholipid biosynthesis. Additionally, we detected phylogenetically unrelated mevalonate pathway genes in metagenome-derived Rickettsiales sequences, likely indicating evolutionary convergent effects of independent horizontal gene transfer events. Accordingly, convergence, involving both gene acquisitions and losses, is highlighted as a relevant evolutionary phenomenon in Rickettsiales, possibly favoured by plasticity and comparable lifestyles, representing a potentially hidden origin of other more nuanced similarities among sub-lineages. This article is protected by copyright. All rights reserved.
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the hidden world of Rickettsiales symbionts candidatus spectririckettsia obscura a novel bacterium found in brazilian and indian paramecium caudatum
Microbial Ecology, 2019Co-Authors: Michele Castelli, Valentina Serra, Marcus Vinicius Xavier Senra, Charan Kumar Basuri, Carlos A G Soares, Sergei I Fokin, Letizia ModeoAbstract:Symbioses between bacteria and eukaryotes are widespread and may have significant impact on the evolutionary history of symbiotic partners. The order Rickettsiales is a lineage of intracellular Alphaproteobacteria characterized by an obligate association with a wide range of eukaryotic hosts, including several unicellular organisms, such as ciliates and amoebas. In this work, we characterized the Rickettsiales symbionts associated with two different genotypes of the freshwater ciliate Paramecium caudatum originated from freshwater environments in distant geographical areas. Phylogenetic analyses based on 16S rRNA gene showed that the two symbionts are closely related to each other (99.4% identity), belong to the family Rickettsiaceae, but are far-related with respect to previously characterized Rickettsiales. Consequently, they were assigned to a new species of a novel genus, namely “Candidatus Spectririckettsia obscura.” Screening on a database of short reads from 16S rRNA gene amplicon-based profiling studies confirmed that bacterial sequences related to the new symbiont are preferentially retrieved from freshwater environments, apparently with extremely scarce occurrence (< 0.1% positive samples). The present work provides new information on the still under-explored biodiversity of Rickettsiales, in particular those associated to ciliate host cells.
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deianiraea an extracellular bacterium associated with the ciliate paramecium suggests an alternative scenario for the evolution of Rickettsiales
The ISME Journal, 2019Co-Authors: Michele Castelli, Letizia Modeo, Elena Sabaneyeva, Olivia Lanzoni, Natalia Lebedeva, Anna Maria Floriano, Stefano Gaiarsa, Konstantin A Benken, Claudio Bandi, Alexey PotekhinAbstract:Rickettsiales are a lineage of obligate 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 synthesise 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 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.
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the extracellular association of the bacterium candidatus deianiraea vastatrix with the ciliate paramecium suggests an alternative scenario for the evolution of Rickettsiales
bioRxiv, 2018Co-Authors: Michele Castelli, Letizia Modeo, Elena Sabaneyeva, Olivia Lanzoni, Natalia Lebedeva, Anna Maria Floriano, Stefano Gaiarsa, Konstantin A Benken, Claudio Bandi, Alexey PotekhinAbstract: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 .
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the genome sequence of candidatus fokinia solitaria insights on reductive evolution in Rickettsiales
Genome Biology and Evolution, 2018Co-Authors: Anna Maria Floriano, Giulio Petroni, Michele Castelli, Sascha Krenek, Thomas U Berendonk, C Bazzocchi, Davide SasseraAbstract:"Candidatus Fokinia solitaria" is an obligate intracellular endosymbiont of a unicellular eukaryote, a ciliate of the genus Paramecium. Here, we present the genome sequence of this bacterium and subsequent analysis. Phylogenomic analysis confirmed the previously reported positioning of the symbiont within the "Candidatus Midichloriaceae" family (order Rickettsiales), as well as its high sequence divergence from other members of the family, indicative of fast sequence evolution. Consistently with this high evolutionary rate, a comparative genomic analysis revealed that the genome of this symbiont is the smallest of the Rickettsiales to date. The reduced genome does not present flagellar genes, nor the pathway for the biosynthesis of lipopolysaccharides (present in all the other so far sequenced members of the family "Candidatus Midichloriaceae") or genes for the Krebs cycle (present, although not always complete, in Rickettsiales). These results indicate an evolutionary trend toward a stronger dependence on the host, in comparison with other members of the family. Two alternative scenarios are compatible with our results; "Candidatus Fokinia solitaria" could be either a recently evolved, vertically transmitted mutualist, or a parasite with a high host-specificity.
Yong-zhen Zhang - One of the best experts on this subject based on the ideXlab platform.
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epidemiology and diversity of Rickettsiales bacteria in humans and animals in jiangsu and jiangxi provinces china
Scientific Reports, 2019Co-Authors: Yong Liao, Yong-zhen Zhang, Edward C Holmes, Jinjin Shen, Yinzhong ChenAbstract:Diseases caused by Rickettsiales bacteria are a global public health problem. To better understand the diversity and origins of Rickettsiales infection in humans and animals, we sampled 134 febrile patients, 173 rodents and 43 shrews, as well as 358 ticks, from two cities in Jiangsu and Jiangxi provinces, China. Our data revealed a relatively high prevalence of scrub typhus cases in both localities. In addition, both serological tests and genetic analysis identified three patients infected with Anaplasma bovis, Rickettsia monacensis, and Orientia tsutsugamushi bacteria. Molecular epidemiological investigation revealed the co-circulation of multiple species of Rickettsiales bacteria in small mammals and ticks in both provinces, potentially including novel bacterial species. In sum, these data demonstrate the ongoing importance of Rickettsiales infection in China and highlight the need for the regular surveillance of local arthropods, mammals and humans.
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extensive diversity of Rickettsiales bacteria in ticks from wuhan china
Ticks and Tick-borne Diseases, 2017Co-Authors: Junhua Tian, Wenping Guo, Edward C Holmes, Yong-zhen ZhangAbstract:Rickettsiales bacteria are important agents of (re)emerging infectious diseases, with ticks playing a key role in their evolution and transmission. We collected 1079 hard ticks belonging to five species (Ixodes sinensis, Rhipicephalus microplus, Haemaphysalis flava, Haemaphysalis hystricis and Haemaphysalis longicornis) from cattle and goats in Wuhan city, Hubei province, China. The dominant tick species was H. longicornis (578, 53.57%), followed by R. microplus (354, 32.81%), H. hystricis (62, 5.75%), H. flava (57, 5.28%), and I. sinensis (28, 2.59%). Rickettsiales bacteria were identified in these ticks by amplifying the Rickettsiales 16S rRNA (rrs), citrate synthase (gltA), and heat shock protein (groEL) genes. The rrs gene of Rickettsiales was positive in 32 (2.97%) ticks, including 2 cases of co-infection, with 4 (0.69%) in H. longicornis, 15 (4.24%) in R. microplus, 7 (12.28%) in H. flava, 1 (1.61%) in H. hystricis, and 5 (17.86%) in I. sinensis ticks. Phylogenetic analysis revealed the presence of six recognized and seven Candidatus species of Rickettsiaceae, Anaplasmataceae and Candidatus Midichloriaceae. Notably, one lineage within both Ehrlichia and Candidatus Midichloriaceae was distinct from any known Rickettsiales, suggesting the presence of potentially novel species of Rickettsiales bacteria. In sum, these data reveal an extensive diversity of Rickettsiales in ticks from Wuhan, highlighting the need to understand Rickettsiales infection in local animals and humans.
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extensive genetic diversity of Rickettsiales bacteria in multiple mosquito species
Scientific Reports, 2016Co-Authors: Wenping Guo, Stephen J. Dumler, Xiao-ping Chen, Junhua Tian, Edward C Holmes, Xian Dan Lin, Yong Liao, Si Yuan Yang, Yong-zhen ZhangAbstract:Rickettsiales are important zoonotic pathogens, causing severe disease in humans globally. Although mosquitoes are an important vector for diverse pathogens, with the exception of members of the genus Wolbachia little is known about their role in the transmission of Rickettsiales. Herein, Rickettsiales were identified by PCR in five species of mosquitoes (Anopheles sinensis, Armigeres subalbatus, Aedes albopictus, Culex quinquefasciatus and Cu. tritaeniorhynchus) collected from three Chinese provinces during 2014-2015. Subsequent phylogenetic analyses of the rrs, groEL and gltA genes revealed the presence of Anaplasma, Ehrlichia, Candidatus Neoehrlichia, and Rickettsia bacteria in mosquitoes, comprising nine documented and five tentative species bacteria, as well as three symbionts/endosybionts. In addition, bacteria were identified in mosquito eggs, larvae, and pupae sampled from aquatic environments. Hence, these data suggest that Rickettsiales circulate widely in mosquitoes in nature. Also of note was that Ehrlichia and Rickettsia bacteria were detected in each life stage of laboratory cultured mosquitoes, suggesting that Rickettsiales may be maintained in mosquitoes through both transstadial and transovarial transmission. In sum, these data indicate that mosquitoes may have played an important role in the transmission and evolution of Rickettsiales in nature.
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Co-circulation of multiple species of Rickettsiales bacteria in one single species of hard ticks in Shenyang, China.
Ticks and tick-borne diseases, 2014Co-Authors: Xue Dong, Stephen J. Dumler, Xiao-ping Chen, Na Liu, Yong-zhen ZhangAbstract:Bacteria in the order Rickettsiales include some of the most important zoonotic (re)emerging pathogens for animals and humans. In 2012, a total of 1267 adult Haemaphysalis longicornis ticks were collected from domestic animals (cattle and sheep) in Shenyang of Liaoning Province, China. These ticks were grouped into 181 pools (each pool with 6-7 ticks). Rickettsiales agents were identified in 93 (51.38%) tick pools using PCR targeting rrs (16S rRNA). In addition to 16S rRNA gene sequences, gltA and groEL gene sequences were also recovered from these positive samples. Phylogenetic analyses of these sequences revealed the presence of five species of Rickettsiales bacteria in a single tick species (H. longicornis) in nature in Shenyang, including Rickettsia japonica, Rickettsia raoultii, Anaplasma centrale, Anaplasma bovis, and a potentially novel A. phagocytophilum variant. Additionally, two Candidatus Ehrlichia spp. (Ehrlichia sp. Yonaguni138, Candidatus Ehrlichia shimanensis) were also identified in these ticks, with the highest prevalence of Ehrlichia sp. Yonaguni138 (73/181, 40.3%). Notably, these agents except the novel A. phagocytophilum variant had close evolutionary relationships with those previously identified in northeastern Asian countries including Korea, Japan, and Russia, indicating a geographic clustering pattern. Our data also reinforce the need for vigilance in recognition and prevention of rickettsiosis, ehrlichiosis, and anaplasmosis in humans and animals in this region.
Deron E. Burkepile - One of the best experts on this subject based on the ideXlab platform.
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Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov
The ISME Journal, 2019Co-Authors: J. Grace Klinges, Elizabeth C. Shaver, Esther C Peters, Stephanie M Rosales, Ryan Mcminds, Koty H. Sharp, Andrew A. Shantz, Michael Eitel, Gert Wörheide, Deron E. BurkepileAbstract:Bacterial symbionts are integral to the health and homeostasis of invertebrate hosts. Notably, members of the Rickettsiales genus Wolbachia influence several aspects of the fitness and evolution of their terrestrial hosts, but few analogous partnerships have been found in marine systems. We report here the genome, phylogenetics, and biogeography of a ubiquitous and novel Rickettsiales species that primarily associates with marine organisms. We previously showed that this bacterium was found in scleractinian corals, responds to nutrient exposure, and is associated with reduced host growth and increased mortality. This bacterium, like other Rickettsiales, has a reduced genome indicative of a parasitic lifestyle. Phylogenetic analysis places this Rickettsiales within a new genus we define as “ Candidatus Aquarickettsia.” Using data from the Earth Microbiome Project and SRA databases, we also demonstrate that members of “ Ca . Aquarickettsia” are found globally in dozens of invertebrate lineages. The coral-associated “ Candidatus A. rohweri” is the first finished genome in this new clade. “ Ca . A. rohweri” lacks genes to synthesize most sugars and amino acids but possesses several genes linked to pathogenicity including Tlc, an antiporter that exchanges host ATP for ADP, and a complete Type IV secretion system. Despite its inability to metabolize nitrogen, “ Ca . A. rohweri” possesses the NtrY-NtrX two-component system involved in sensing and responding to extracellular nitrogen. Given these data, along with visualization of the parasite in host tissues, we hypothesize that “ Ca . A. rohweri” reduces coral health by consuming host nutrients and energy, thus weakening and eventually killing host cells. Last, we hypothesize that nutrient enrichment, which is increasingly common on coral reefs, encourages unrestricted growth of “ Ca . A. rohweri” in its host by providing abundant N-rich metabolites to be scavenged.
Letizia Modeo - One of the best experts on this subject based on the ideXlab platform.
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candidatus sarmatiella mevalonica endosymbiont of the ciliate paramecium provides insights on evolutionary plasticity among Rickettsiales
Environmental Microbiology, 2021Co-Authors: Michele Castelli, Letizia Modeo, Olivia Lanzoni, Alexey Potekhin, Davide Sassera, Tiago Nardi, Stefano Lometto, Giulio PetroniAbstract:Members of the bacterial order Rickettsiales are obligatorily associated with a wide range of eukaryotic hosts. Their evolutionary trajectories, in particular concerning the origin of shared or differential traits among distant sub-lineages, are still poorly understood. Here we characterised a novel Rickettsiales bacterium associated with the ciliate Paramecium tredecaurelia, and phylogenetically related to the Rickettsia genus. Its genome encodes significant lineage-specific features, chiefly the mevalonate pathway gene repertoire, involved in isoprenoid precursor biosynthesis. Not only this pathway has never been described in Rickettsiales, it also is very rare among bacteria, though typical in eukaryotes, thus likely representing a horizontally-acquired trait. The presence of these genes could enable an efficient exploitation of host-derived intermediates for isoprenoid synthesis. Moreover, we hypothesise the reversed reactions could have replaced canonical pathways for producing acetyl-CoA, essential for phospholipid biosynthesis. Additionally, we detected phylogenetically unrelated mevalonate pathway genes in metagenome-derived Rickettsiales sequences, likely indicating evolutionary convergent effects of independent horizontal gene transfer events. Accordingly, convergence, involving both gene acquisitions and losses, is highlighted as a relevant evolutionary phenomenon in Rickettsiales, possibly favoured by plasticity and comparable lifestyles, representing a potentially hidden origin of other more nuanced similarities among sub-lineages. This article is protected by copyright. All rights reserved.
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the hidden world of Rickettsiales symbionts candidatus spectririckettsia obscura a novel bacterium found in brazilian and indian paramecium caudatum
Microbial Ecology, 2019Co-Authors: Michele Castelli, Valentina Serra, Marcus Vinicius Xavier Senra, Charan Kumar Basuri, Carlos A G Soares, Sergei I Fokin, Letizia ModeoAbstract:Symbioses between bacteria and eukaryotes are widespread and may have significant impact on the evolutionary history of symbiotic partners. The order Rickettsiales is a lineage of intracellular Alphaproteobacteria characterized by an obligate association with a wide range of eukaryotic hosts, including several unicellular organisms, such as ciliates and amoebas. In this work, we characterized the Rickettsiales symbionts associated with two different genotypes of the freshwater ciliate Paramecium caudatum originated from freshwater environments in distant geographical areas. Phylogenetic analyses based on 16S rRNA gene showed that the two symbionts are closely related to each other (99.4% identity), belong to the family Rickettsiaceae, but are far-related with respect to previously characterized Rickettsiales. Consequently, they were assigned to a new species of a novel genus, namely “Candidatus Spectririckettsia obscura.” Screening on a database of short reads from 16S rRNA gene amplicon-based profiling studies confirmed that bacterial sequences related to the new symbiont are preferentially retrieved from freshwater environments, apparently with extremely scarce occurrence (< 0.1% positive samples). The present work provides new information on the still under-explored biodiversity of Rickettsiales, in particular those associated to ciliate host cells.
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deianiraea an extracellular bacterium associated with the ciliate paramecium suggests an alternative scenario for the evolution of Rickettsiales
The ISME Journal, 2019Co-Authors: Michele Castelli, Letizia Modeo, Elena Sabaneyeva, Olivia Lanzoni, Natalia Lebedeva, Anna Maria Floriano, Stefano Gaiarsa, Konstantin A Benken, Claudio Bandi, Alexey PotekhinAbstract:Rickettsiales are a lineage of obligate 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 synthesise 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 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.
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the extracellular association of the bacterium candidatus deianiraea vastatrix with the ciliate paramecium suggests an alternative scenario for the evolution of Rickettsiales
bioRxiv, 2018Co-Authors: Michele Castelli, Letizia Modeo, Elena Sabaneyeva, Olivia Lanzoni, Natalia Lebedeva, Anna Maria Floriano, Stefano Gaiarsa, Konstantin A Benken, Claudio Bandi, Alexey PotekhinAbstract: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 .
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Protist ciliates as natural reservoir for bacteria potentially pathogenic for metazoan: preliminary results of the experimental infection of the planarian Dugesia.
2016Co-Authors: Letizia Modeo, Di Giuseppe Graziano, Alessandra Salvetti, Leonardo Rossi, Claudia Vannini, Sergey Fokin, Giulio Petroni, Franco VerniAbstract:Most of the microorganisms belonging to genera responsible for vector-borne diseases (VBD) has hematophagous arthropods as vector/reservoir. Recently, many new species of such microorganisms were found in a variety of terrestrial and aquatic eukaryotic hosts: in particular, numerous new bacterial species belonging/related to the genus Rickettsia, Alphaproteobacteria of the order Rickettsiales with an obligate intracellular lifestyle (e.g. the etiological agents of epidemic typhus and spotted fever), were discovered in protist ciliates. Although their pathogenicity for either humans or animals is still under study, these bacteria could actually act as etiological agents of possible VBD of aquatic environment. Indeed, an increasing number of massive fish death was recorded in intensive aquaculture facilities during the lasts years due to epidemics caused by Rickettsia-like bacteria with unknown natural vector. As ciliates could vector pathogenic organisms possibly responsible for zoonosis, we intended to verify the transmission of the Rickettsiales endosymbionts hosted by two species of ciliates to a metazoan model, the planarian Dugesia japonica. The ciliates were Euplotes woodruffi and Paramecium multimicronucleatum; the first hosts in the cytoplasm two different Rickettsiales endosymbionts, “Candidatus (Ca) Megaira polyxenophila” and “Ca. Bandiella woodruffii”, in addition to the betaproteobacterium Polynucleobacter necessarius; the second hosts in the macronucleus the Rickettsiales endosymbiont “Ca. Trichorickettsia mobilis”. Ciliate monoclonal mass cultures were set up to perform the following infection experiments: 1. Ciliate washing, concentrating, homogenizing, and addition to regular food for planarians. 2. Antibiotic-treated planarians feeding on ciliate-enriched food or regular food (as control), then washing and letting digest for 24, 48, and 72 h; 3. Comparative multidisciplinary investigation: molecular analyses, whole mount in situ hybridization, and TEM observation. Preliminary results are encouraging: we recovered endosymbionts up to 72 h after feeding, and identified them in planarians’ intestine and digestive vacuoles in TEM material. Endosymbionts were frequently observed near vacuole edge, with vacuole membrane sometimes somehow interrupted. TEM results were compared with literature data where endosymbionts were demonstrated to escape vacuoles invading the cytoplasm. Financial support: PRA 2016, University of Pisa
