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Husnik, F.

Publications and source records attributed to Husnik, F..

18 recordsLinked to original sources

Comparing Symbiodiniaceae diversity across unicellular hosts, multicellular hosts, and environmental reservoirs

Symbiodiniaceae dinoflagellates are the primary photosymbionts in reef ecosystems, crucial for reef productivity. Although they are widely recognized as symbionts of animals such as corals and clams, they can occupy a broad range of reef niches, including water, sediment, and macroalgae. Understanding their ecology is typically hampered by their horizontal acquisition. Combining evidence from multiple sample types collected at the same location has the potential to address this issue, but such analyses are surprisingly rare. Here, we analysed Symbiodiniaceae communities across 74 environmental and host samples in one reef flat in Okinawa, Japan. We detected ten Symbiodiniaceae genera or genus-level clades using the ITS2 marker metabarcoding, including Clade J, previously known only from Okinotori Island, Japan. Cladocopium, Symbiodinium, and Durusdinium dominated multicellular hosts (hexacorals and Tridacna). In contrast, foraminiferal hosts were dominated by Cladocopium or genus-specific Freudenthalidium, Fugacium, and Miliolidium. Symbiont communities were mostly specific to the host genera. Water samples, with higher proportions of Durusdinium and free-living Symbiodinium, were distinct from macroalgae and sediment samples. The latter did not differ significantly from each other and contained Freudenthalidium, Fugacium, Miliolidium, Clade I, and Clade J. Only three ITS2 variants were shared across all sample categories, but many variants were unique to hosts or habitats. We highlight that both unicellular and multicellular hosts harbor specific endosymbiont types, with lower diversity than in the surrounding environment. Our results imply that host diversity, availability, and environmental context jointly structure photosymbiont communities at fine spatial scales within coral reef ecosystems.

microbiology↗

The colourless dictyochophyte Ciliophrys sp. Baltic secondarily lacks a plastid but hosts a bacterial endosymbiont

The loss of an organelle represents an extreme case of reductive evolution. Only a few plastid loss events have been documented and they seem to be particularly rare in free-living ancestrally photosynthetic taxa. We isolated a new phagotrophic protist, Ciliophrys sp. Baltic, representing a poorly studied non-photosynthetic lineage in the stramenopile algal class Dictyochophyceae. Genomic and transcriptomic data from this organism demonstrate that it lacks a plastid genome and nuclear genes critical for plastid biogenesis. The plastid organelle is thus most likely secondarily missing from Ciliophrys sp. Baltic, although a few enzymes originally targeted to the plastid persist with a changed localization. Unexpectedly, Ciliophrys sp. Baltic harbors a bacterial endosymbiont, Candidatus Penulousia baltica sp. nov. (Rickettsiales). Analysis of its complete genome sequence uncovered unique aspects of its metabolism not previously reported in other Rickettsiales. The bacterium exploits its host metabolically and presumably manipulates it with an arsenal of putative effector proteins. However, we also found that it might help offset some of the biosynthetic deficiencies of its host stemming from the plastid loss by providing haem and a lysine precursor. Altogether, our study establishes a new single-cell model system for studying plastid loss and endosymbiont acquisition.

evolutionary biology↗

Parallel Evolution of Bacteroidota as Long-Term Endosymbionts of Insects

Symbiotic relationships transform diverse aspects of both symbiont and host biology. The most visible changes include a massive reduction of the endosymbiont genome and the development of novel host organs, cells, and compartments specialized for harboring the symbionts. However, many insect symbiosis studies have previously focused either on Proteo-bacteria or only on a particular symbiosis stage, limiting our broad understanding of how and why symbiont diversity arises from specific microbial clades, how the symbiont genomes erode over evolutionary time, and what the consequences of symbiosis are for diverse host-symbiont pairs. Thanks to the repeated gains and losses of nutritional symbionts, scale insects provide an ideal evolutionary playground for tracking the parallel transitions of insect symbionts that originated as independent evolutionary replicates from the same bacterial phylum. Using extensive genome sampling across the scale insect phylogeny, we recapitulated the path of Bacteroidota transitioning from recently established host-associated bacteria to highly specialized insect endosymbionts with minimal gene sets. Their genomes exhibit strikingly parallel patterns of gene loss and pseudogenization across all gene categories, with some stochastic differences in essential genes for genetic processing and amino acid biosynthesis. In addition to the genetic transition, we show with imaging methods that the symbiotic cells and organs exhibit a trend from more dispersed bacteriocytes to highly compact (and likely more specialized) bacteriomes, which are closely localized to the hosts digestive system. Our results outline at both genomic and cellular levels a recurrent path by which insect symbioses independently arise, are temporarily maintained for up to several hundred million years, and then are replaced by new symbionts that repeat the process. The gradual nature of the process implies that the outcomes of symbiosis initially depend on how professional vs. naive the host and symbiont are. Over evolutionary time, compatible host-symbiont lineages emerge from these interactions and become preferred.

evolutionary biology↗

Genomic diversity and functional potential of facultative bacterial symbionts across scale insects

Microbial symbionts play pivotal roles in the physiology, ecology, and evolution of insects. While obligate symbionts have been extensively characterized in insects feeding on nutritionally poor diets, the diversity and functional roles of facultative bacterial symbionts remain largely unexplored in many insect lineages, including scale insects (Hemiptera: Coccomorpha). Here, we present a genome-resolved metagenomic and comparative genomic analysis of facultative bacterial symbionts across 120 scale insect metagenomes from 20 different families. Our analyses reveal rich and taxonomically diverse facultative symbiont communities, dominated by the Pseudomonadota, such as Wolbachia, Rickettsia, Arsenophonus, and Sodalis. Genomic features reveal substantial variation in genome sizes, coding densities, metabolic potentials, and hostinteraction genes among symbiont clades, indicating lineage-specific lifestyles and host interactions. Interestingly, alphaproteobacterial and gammaproteobacterial symbionts mostly co-occur within their respective hosts. Gammaproteobacterial symbionts exhibit broader metabolic repertoires and potential defense capabilities via the APSE phage toxin cassettes, while alphaproteobacterial symbionts retain reduced metabolic capabilities, Type IV secretion systems, and reproductive manipulation genes (cifAB and wmk). We propose how the symbiont genes related to nutritional provisioning, defensive symbiosis, and reproductive manipulation may influence the biology and evolution of scale insects. Our results provide the first comprehensive genomic overview of facultative bacterial symbionts in scale insects, revealing their evolutionary dynamics and putative functions.

genomics↗

Non-photosynthetic Plastid Replacement by a Primary Plastid in the Making

The integration of a cyanobacterium into a heterotrophic eukaryote gave rise to the primary plastid [~]1.5 Gya. This rare cyanobacterium-to-plastid transition has only been reported once more in Paulinella chromatophora [~]100 Mya. Unfortunately, the order and relative importance of organellogenesis events have been blurred by time in primary plastids and obscured by P. chromatophora becoming phototrophic. Here, we characterize the tripartite symbiosis in a benthic dinoflagellate (Sinophysis sp.) using diverse single-cell methods. Sinophysis houses a photosynthetic cyanobacterium closely interacting with an alphaproteobacterial endosymbiont. The cyanobacterium is in the intermediate stage of symbiont-to-organelle transition, with the host likely supporting it with metabolites and proteins, and controlling its cell division. Surprisingly, it seems to have replaced the hosts remnant non-photosynthetic plastid. Our results support mixotrophy, horizontal gene transfer, co-symbioses, and cell division control as early drivers of primary plastid origin and highlight the importance of protists for deciphering organellogenesis events.

evolutionary biology↗

A Midichloriaceae endosymbiont of terrestrial arthropods found as an endosymbiont in a marine nematode

The obligate endosymbiont Candidatus Lariskella (Alphaproteobacteria, Candidatus Midichloriaceae) has been found across a wide diversity of terrestrial arthropods, including ticks, true bugs, beetles, fleas, wasps and moths. However, to date, Ca. Lariskella had never been detected in nematodes or marine animals. Here we report the first known occurrence of Ca. Lariskella infecting a population of marine nematodes (Enoplida, Thoracostomopsideae). This nematode-infecting Ca. Lariskella is closely related to insect-infecting Ca. Lariskella, despite the drastic shift in both host phylum and habitat. TEM and FISH microscopy showed Ca. Lariskella is localized within both somatic cells and developing oocytes, strongly suggesting that Ca. Lariskella is a vertically transmitted endosymbiont within the nematode population. We found that Ca. Lariskella was present within approximately 20% of the nematode population, but notably failed to detect any Ca. Lariskella within adult males, potentially hinting at reproductive manipulation. Overall, our findings show that Ca. Lariskella is not limited to arthropods or terrestrial hosts, indicating a larger host range than previously described. Its presence within marine nematodes demonstrates the ability of Ca. Lariskella to infect nematode hosts, as well as hosts from marine environments, suggesting terrestrial nematodes, marine arthropods, and perhaps even other marine invertebrates could be potential hosts of Ca. Lariskella.

microbiology↗

Phylogenomics clarifies Balanophora evolution, plastid reduction, and obligate asexuality origins

Holoparasitic plants are non-green plants that depend entirely on their host plants for essential resources, which often results in functional reduction and gene loss. However, the timing and extent of gene loss associated with parasitism remain unclear. Although Balanaphara is known to have highly reduced plastid genomes, only five species from a few geographically restricted regions have been studied. Here, we expanded Balanaphara sampling with seven species from twelve populations across Taiwan and Japan. We assembled their plastid genomes and transcriptomes and inferred multi-gene phylogenies from diverse plastid and nuclear markers. The uncovered relationships within the genus imply independent origins of obligate apomixis in island populations of several species. All the plastid genomes are highly reduced (14-16 kbp), gene-dense, completely syntenic, strongly AT-biased (87-88%), and with the same non-canonical genetic code (TAG->Trp) as previously reported in other Balanaphara species. To further understand the functional role of these non-photosynthetic plastids, we predicted the subcellular localization of nuclear-encoded proteins based on expression data. Strikingly, over 800 Balanaphara proteins were predicted to be plastid-targeted, suggesting a retained capacity for the biosynthesis of amino acids, fatty acids, riboflavin, lipoic acid, heme, isoprenoids, and components of the glycolysis and pentose phosphate pathways. Our findings show that the extreme plastid genome reduction in Balanaphara mainly occurred before the origin of the clade and primarily erased photosynthesis-related functions. Numerous highly expressed nuclear genes of Balanaphara still retain chloroplast transit peptides, and the resulting proteins are likely targeted to the non-photosynthetic organelle that remains metabolically active. Similar to other parasitic eukaryotes with non-photosynthetic plastids, such as apicomplexans, the loss of photosynthesis led to extreme plastid genome reduction without massive elimination of other photosynthesis-unrelated functions. Balanophoraceae thus emerges as a fascinating model for reconstructing the evolutionary changes associated with photosynthesis loss in land plants.

evolutionary biology↗

Horizontal gene transfers are widespread across termite genomes but do not confer metabolic innovations

Horizontal gene transfer (HGT), the transmission of genetic material across species, is an important innovation source in prokaryotes. In contrast, its significance is unclear in many eukaryotes, including insects. Here, we used high-quality genomes of 45 termites and two cockroaches to investigate HGTs across blattodean genomes. We identified 289 genes and 2,494 pseudogenes classified into 168 orthologous groups originating from an estimated 281 HGT events. Wolbachia represented the primary HGT source, while termite gut bacteria and the cockroach endosymbiont Blattabacterium did not contribute meaningfully to HGTs. Most horizontally acquired genes descended from recent and species-specific HGTs, experienced frequent duplications and pseudogenizations, and accumulated substitutions faster than synonymous sites of native protein-coding genes. Genes frequently transferred horizontally to termite genomes included mobile genetic elements and genetic information processing genes. Our results indicate that termites continuously acquired genes through HGT, which they soon lost, leaving few horizontally acquired genes conserved across lineages.

genomics↗

Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iotorishima Island

Ocean acidification (OA), driven by rising atmospheric CO2, presents a serious threat to marine biodiversity, especially within coral reef ecosystems. Natural analogue sites, such as the high-pCO2 seep at I[o]torishima Island in Japan, offer insights into future conditions. This study investigated the holobiont communities of Symbiodiniaceae and bacteria in the zoantharian Palythoa tuberculosa at I[o]torishima and compared them to specimens from control sites in Okinawa and Hawaii. Using amplicon sequencing of the dinoflagellate internal transcribed spacer 2 (ITS2) region of ribosomal DNA and microbial 16S rRNA gene, we detected significant shifts in both Symbiodiniaceae and bacterial communities under high-pCO2 conditions at I[o]torishima. Specifically, P. tuberculosa at the seep site had reduced Symbiodiniaceae diversity, predominatly featuring Cladocopium C1 and C3 types. Additionally, its bacterial communities showed lower richness with distinct taxonomic profiles, including increased levels of Mollicutes and Vibrio spp. These results highlight the potentially adverse effects of OA on hexacoral holobionts and emphasize the need for detailed, high-resolution studies across various holobiont species and geographic locations. The shifts observed specifically in Symbiodiniaceae and bacterial communities at the I[o]torishima Seep suggest that holobionts may exhibit plasticity in response to environmental stress, which has implications for resilience and adaptation of zoantharians and other reef organisms amid climate change. This research provides crucial baseline data for predicting future coral reef compositions in an OA-affected world.

microbiology↗

The diversification of mealybugs was triggered by new symbiont acquisitions and followed by adaptive radiations on host plants

Symbiotic microorganisms play a critical role in supplementing beneficial nutrients to herbivorous insects feeding on unbalanced diets. These microbial symbionts can both facilitate or constrain plant-feeding insects adaptations to certain host plants, depending on their gene content and metabolic potential. The diet breadth of herbivorous insects is considered an important evolutionary factor affecting genotypic and phenotypic changes associated with host shifts. Acquiring new symbionts can, therefore, drive changes in niche breadth and subsequent adaptive radiation(s). Mealybugs comprise one of the major groups of scale insects, most of which feed on diverse angiosperms. Different sub-lineages of mealybugs also house different lineages of bacteria and fungi as their obligate symbionts. Here, we use mealybugs as a model system to test the hypothesis that the evolution of herbivorous insects is driven by both obligate symbionts and host plants. Based on metagenome analyses of 28 host species as well as a literature survey, we identified Betaproteobacteria, Gammaproteobacteria, Flavobacteriia, and Ophiocordyceps fungi as obligate symbionts of the major clades of mealybugs. A time-calibrated phylogenetic tree of mealybugs allowed us to infer the ancestral obligate symbionts of the major mealybug clades. Our results indicate that the emergence of major mealybug lineages coincided with the acquisitions of new obligate endosymbionts. Subsequent radiations of mealybugs were inferred to have mostly resulted from the adaptive radiation through continuous host shifts on angiosperms. The contribution of microbial symbiosis to the diversification of herbivorous insects is thus likely limited by new symbiont origins or replacements, and insect adaptations play a larger role in further plant switches.

evolutionary biology↗

Accelerated pseudogenization in ancient endosymbionts of giant scale insects

Symbiotic microorganisms are subject to a complex interplay of environmental and population-genetic pressures that drive their gene loss. Despite the widely held perception that ancient symbionts have stable genomes, even tiny genomes experience ongoing pseudogenization. Whether these tiny genomes also experience bursts of rapid gene loss is, however, less understood. Giant scale insects (Monophlebidae) feed on plant sap and rely on the symbiotic bacterium Walczuchella which provides them with essential nutrients. When compared to other ancient symbionts with similar genome sizes such as Karelsulcia, Walczuchellas genome was previously reported as unusually pseudogene-rich (10 % of coding sequences). However, this result was based on only one genome assembly raising questions about the assembly quality or a recent ecological shift such as co-symbiont acquisition driving the gene loss. Here, we generated six complete genomes of Walczuchella from three genera of giant scales, each with distinct co-symbiotic partners. We show that all the genomes are highly degraded and particularly genes related to the cellular envelope and energy metabolism seem to be ongoing pseudogenization. Apart from general mechanisms driving genome reduction such as the long-term intracellular lifestyle with transmission bottlenecks, we hypothesize that a more profound loss of DNA replication and repair genes together with recent co-obligate symbiont acquisitions likely contribute to the accelerated degradation of Walczuchella genomes. Our results highlight that even ancient symbionts with small genomes can experience significant bursts of gene loss when stochastic processes erase a gene that accelerates gene loss or when the selection pressure changes such as after cosymbiont acquisition.

genomics↗

Charting the landscape of cytoskeletal diversity in microbial eukaryotes

Microbial eukaryotes are small and often resistant to standard labelling and imaging techniques, and therefore remain understudied - despite their critical ecological importance - with the exception of a few established models. Here, we use Ultrastructure Expansion Microscopy (U-ExM) to carry out high-resolution volumetric imaging of over 200 cultured planktonic eukaryotes across major lineages. By combining U-ExM with pan- and specific immuno-labelling, we reveal novel microtubule and centrin-containing elements and assign molecular identities to enigmatic cytoskeletal structures observed previously only by electron microscopy. Our investigation represents the first systematic survey of the extensive cytoskeletal diversity on display across the eukaryotic tree, including the major species groups of dinoflagellates, haptophytes, ciliates, euglenids, cryptomonads, and green algae. Our U-ExM approach extends to mixed environmental samples, paving the way for environmental cell biology at ultrastructural resolution and unprecedented scale, a crucial step towards understanding and protecting complex ecosystems in the face of biodiversity loss.

cell biology↗

Coral microbiomes from the Atlantic and Indo-Pacific oceans have the same alpha diversity but different composition

Corals are early-branching animals highly reliant on diverse symbionts for growth and reproduction. Most coral groups, including stony corals and hydrocorals, exhibit deep genetic divergence between the Atlantic (ATO) and Indo-Pacific (IPO) oceans, hampering their direct comparison. Although sibling zoanthid species (Hexacorallia: Zoantharia) deviate from this pattern, their symbioses have so far only been studied on local scales. Here, we examined the microbiomes of Palythoa caribaeorum from the ATO and P. tuberculosa from the IPO. Our extensive geographical sampling and metabarcoding revealed that Palythoa microbiomes have similar alpha diversity in both oceans. The primary exceptions are the symbiodiniacean Cladocopium and Chlamydiae bacteria, which mirror the global diversity patterns of corals. Despite distinct overall microbial compositions between oceans, some regions shared remarkably similar communities, hinting at the importance of both symbiont phylogeny and function. Finally, we explore the shift from commensal/mutualistic microbes to opportunistic pathogens, crucial amid the ongoing environmental changes.

microbiology↗

Pseudofinder: detection of pseudogenes in prokaryotic genomes

Prokaryotic genomes are generally gene dense and encode relatively few pseudogenes, or nonfunctional/inactivated remnants of genes. However, in certain contexts, such as recent ecological shifts or extreme population bottlenecks (such as those experienced by symbionts and pathogens), pseudogenes can quickly accumulate and form a substantial fraction of the genome. Identification of pseudogenes is, thus, a critical step for understanding the evolutionary forces acting upon, and the functional potential encoded within, prokaryotic genomes. Here, we present Pseudofinder, an open-source software dedicated to pseudogene identification and analysis. With Pseudofinders multi-pronged, reference-based approach, we demonstrate its capacity to detect a wide variety of pseudogenes, including those that are highly degraded and typically missed by gene-calling pipelines, as well newly formed pseudogenes, which can have only one or a few inactivating mutations. Additionally, Pseudofinder can detect intact genes undergoing relaxed selection, which may indicate incipient pseudogene formation. Implementation of Pseudofinder in annotation pipelines will not only clarify the functional potential of sequenced microbes, but will also generate novel insights and hypotheses regarding the evolutionary dynamics of bacterial and archaeal genomes.

bioinformatics↗

Highly reduced genomes of protist endosymbionts show evolutionary convergence

Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts [1-4]. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems. However, eukaryotic microbes, or protists, also harbor diverse bacterial endosymbionts, but their genome reduction and functional relationships with their more diverse hosts are largely unexplored [5-7]. We sequenced the genomes of four bacterial endosymbionts from three species of diplonemids, poorly-studied but abundant and diverse heterotrophic protists [8-10]. The endosymbionts come from two intracellular families from different orders, Rickettsiaceae and Holosporaceae, that have invaded diplonemids multiple times, and their genomes have converged on an extremely small size (605-632 kbp), similar gene content (e.g., metabolite transporters and secretion systems), and reduced metabolic potential (e.g., loss of energy metabolism). These characteristics are generally found in both families, but the diplonemid endosymbionts have evolved greater extremes in parallel. Their modified type VI secretion systems are likely involved in the manipulation of host metabolism (e.g., interactions with host mitochondria) or defense against bacterial infections, although their similar effector/immunity proteins may also allow for co-occurring Holosporaceae species in one diplonemid host. Finally, modified cellular machinery like ATP synthase without oxidative phosphorylation and reduced flagella present in both diplonemid endosymbionts and nutritional animal endosymbionts indicates that intracellular mechanisms have converged in bacterial endosymbionts with various functions and from different eukaryotic hosts across the tree of life.

evolutionary biology↗

Insect-symbiont gene expression in the midgut bacteriocytes of a blood-sucking parasite

BackgroundAnimals interact with a diverse array of both beneficial and detrimental microorganisms. These interactions sometimes spark obligate symbioses where the host depends on beneficial bacteria for survival and reproduction. In insects, these obligate symbioses in many cases allow feeding on nutritionally unbalanced diets such as plant sap and vertebrate blood. It is, however, still not clear how are these obligate intracellular symbioses maintained at the cellular level for up to several hundred million years. Exact mechanisms driving host-symbiont interactions are only understood for a handful of model species and data on blood-feeding hosts with intracellular bacteria are particularly scarce.\n\nResultsHere, we analyzed interactions at the symbiotic interfaces of an obligately blood-sucking parasite of sheep, the louse fly Melophagus ovinus. We assembled a reference transcriptome from one male and one female individual and used RNA-Seq with five biological replicates to compare expression in the midgut cells housing bacteria to the rest of the gut (foregut-hindgut). We focused on nutritional and immunity interactions between the insect host and its obligate symbiont Arsenophonus melophagi, and also generated lower-coverage data for three facultative bacterial symbionts (Sodalis melophagi, Bartonella melophagi, and Wolbachia sp.) and one facultative eukaryote Trypanosoma melophagium. We found strong evidence for the importance of zinc in the system likely caused by symbionts using zinc-dependent proteases when acquiring amino acids, and for likely different immunity mechanisms controlling the symbionts than in closely related tsetse flies.\n\nConclusionsOur results show that cellular and nutritional interactions between this blood-sucking insect and its symbionts are less intimate than what was previously found in some (but not all) plant-sap sucking insects such as aphids, psyllids, whiteflies, and mealybugs. This finding is likely interconnected to several features observed in symbionts in blood-sucking arthropods, particularly their midgut intracellular localization (as opposed to being localized in truly specialized bacteriocytes), intracytoplasmic presence (as opposed to having an outermost host-derived symbiosomal membrane), less severe genome reduction, and relatively recent associations caused by frequent evolutionary losses and replacements.\n\nData depositionRaw RNA-Seq data were made available through the European Nucleotide Archive (ENA) database under the study accession number PRJEB30632. All assemblies and additional large supplementary files are available on FigShare [https://doi.org/10.6084/m9.figshare.6146777.v1]. All commands used for data analyses are available on Github [https://github.com/filip-husnik/melophagus].

genomics↗

Chromulinavorax destructans, a pathogenic TM6 bacterium with an unusual replication strategy targeting protist mitochondrion

Most of the diversity of microbial life is not available in culture, and as such we lack even a fundamental understanding of the biological diversity of several branches on the tree of life. One branch that is highly underrepresented is the candidate phylum TM6, also known as the Dependentiae. Their biology is known only from reduced genomes recovered from metagenomes around the world and two isolates infecting amoebae, all suggest that they live highly host-associated lifestyles as parasites or symbionts. Chromulinavorax destructans is an isolate from the TM6/Dependentiae that infects and lyses the abundant heterotrophic flagellate, Spumella elongata. Chromulinavorax destructans is characterized by a high degree of reduction and specialization for infection, so much so it was discovered in a screen for giant viruses. Its 1.2 Mb genome shows no metabolic potential and C. destructans instead relies on extensive transporter system to import nutrients, and even energy in the form of ATP from the host. Accordingly, it replicates in a viral-like fashion, while extensively reorganizing and expanding the host mitochondrion. 44% of proteins contain signal sequences for secretion, which includes many proteins of unknown function as well as 98 copies of ankyrin-repeat domain proteins, known effectors of host modulation, suggesting the presence of an extensive host-manipulation apparatus.

microbiology↗

Legionella becoming a mutualist: adaptive processes shaping the genome of symbiont in the louse Polyplax serrata

Legionellaceae are intracellular bacteria known as important pathogens of man. In the environment, they are mainly found in biofilms associated with amoebas. In contrast to another gammaproteobacterial family Enterobacteriaceae which established a broad spectrum of symbioses with many insect taxa, the only instance of legionella-like symbiont has been reported from lice of the genus Polyplax. Here, we sequenced the complete genome of this symbiont and compared its main characteristics to other Legionella species and insect symbionts. Based on rigorous multigene phylogenetic analyses, we confirm this bacterium as a member of the genus Legionella and propose the name Candidatus Legionella polyplacis, sp.n. We show that the genome of Ca. Legionella polyplacis underwent massive degeneration, including considerable size reduction (529.746 bp, 484 protein coding genes) and a severe decrease in GC content (23%). We identify several possible constraints underlying the evolution of this bacterium. On one hand, Ca. Legionella polyplacis and the louse symbionts Riesia and Puchtella experienced convergent evolution, perhaps due to adaptation to similar hosts. On the other hand, some metabolic differences are likely to reflect different phylogenetic positions of the symbionts and hence availability of particular metabolic function in the ancestor. This is exemplified by different arrangements of thiamine metabolism in Ca. Legionella polyplacis and Riesia. Finally, horizontal gene transfer is shown to play a significant role in the adaptive and diversification process. Particularly, we show that Ca. L. polyplacis horizontally acquired a complete biotin operon (bioADCHFB) that likely assisted this bacterium when becoming an obligate mutualist.

evolutionary biology↗