RESUMO
In October 2022, v-shaped necrotic lesions were observed on the leaf margins of field-grown winter oilseed rape (WOSR), Brassica napus L., in western France (Ille-et-Vilaine (35) and Maine-et-Loire (49) departments). Disease incidence on volunteers and cultivated WOSR was generally low (5-10 %) but occasionally up to 80% on some fields. Leaf sections sampled from the margin of necrotic leaf tissue were dilacerated in sterile deionized water and the extract was spread onto tryptone soya agar (TSA) with cycloheximide (100 mg.L-1) and Polyflor (Syngenta, France) (2ml.L-1, containing 5 mg.L-1 propiconazole) then incubated at 28°C for 2 days. Colonies were yellow-pigmented, mucoid, and convex, which are morphological characteristics of Xanthomonas spp. colonies. The partial fyuA and gyrB gene sequences were amplified for eight isolated strains (CFBP 9155, CFBP 9156, CFBP 9157, CFBP 9158, CFBP 9159, CFBP 9161, CFBP 9162, and CFBP 9163) using primers of Fargier et al. (2011), and sequenced (Genoscreen, France). The sequences were deposited under numbers OR232891 to OR232898 for fyuA and OR634932 to OR634939 for gyrB. BLASTN analysis of the sequenced fyuA amplicon showed 100% identity and query coverage with the fyuA fragment of Xanthomonas campestris pv. campestris (Xcc) CFBP 6865R (Bellenot et al., 2022). BLASTN analysis of the sequenced gyrB amplicon showed two allelic forms: one showed 100% identity and query coverage with the gyrB fragment of Xcc strain CFBP 6865R (Bellenot et al., 2022), the other one showed 100% identity and query coverage with the type strain Xcc CFBP 5241 (ATCC33913) (Vorhölter et al., 2003). Moreover, two qPCR tools were used to identify the strains successfully as Xcc (Köhl et al., 2011; Rezki et al., 2016) which target the same gene encoding a hypothetical protein and whose primers overlap. The pathogenicity of the eight isolated strains was validated using a bacterial suspension (108 CFU.ml-1) for i) leaf spraying until runoff onto the leaf surfaces of WOSR plants previously maintained at saturated humidity for 48 hours, ii) wound-leaf inoculation of the two youngest true leaves with scissors that had been dipped into the bacterial suspension. Both tests were performed on 3-week-old WOSR plants of the Aviso (INRAE) genotype. Deionized water was used as negative control. Strains CFBP 5241 and the strain CFBP 4954 (Fargier et al., 2007) were used as positive controls for disease expression. Tested plants (seven for spray inoculation and four for wound-leaf inoculation per strain and control condition) were incubated in a greenhouse at 20°C/24°C (night/day). Isolated strains and the strain CFBP 4954 caused yellow lesions with both inoculation methods that necrotized starting about 10 days post inoculation (dpi). The spots coalesced within 14 dpi to form necrotic areas. The type strain CFBP 5241 caused mild symptoms, with only yellow lesions that did not coalesce. Plants inoculated with water remained symptomless. To complete Koch's postulate, re-isolations were achieved. Re-isolated strains on TSA showed the same colony morphology as described above. All re-isolated strains were identified as Xcc based on partial gyrB sequencing and Xcc specific qPCR test (Rezki et al., 2016). This first report in France and the recent identification in Serbia (Popovic et al., 2013) may illustrate the emergence of the disease on this crop in Europe. The prevalence and consequences of this disease should be evaluated over a wider geographic area.
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Psyllids are phloem-feeding insects that can transmit plant pathogens such as phytoplasmas, intracellular bacteria causing numerous plant diseases worldwide. Their microbiomes are essential for insect physiology and may also influence the capacity of vectors to transmit pathogens. Using 16S rRNA gene metabarcoding, we compared the microbiomes of three sympatric psyllid species associated with pear trees in Central Europe. All three species are able to transmit 'Candidatus Phytoplasma pyri', albeit with different efficiencies. Our results revealed potential relationships between insect biology and microbiome composition that varied during psyllid ontogeny and between generations in Cacopsylla pyri and C. pyricola, as well as between localities in C. pyri. In contrast, no variations related to psyllid life cycle and geography were detected in C. pyrisuga. In addition to the primary endosymbiont Carsonella ruddii, we detected another highly abundant endosymbiont (unclassified Enterobacteriaceae). C. pyri and C. pyricola shared the same taxon of Enterobacteriaceae which is related to endosymbionts harboured by other psyllid species from various families. In contrast, C. pyrisuga carried a different Enterobacteriaceae taxon related to the genus Sodalis. Our study provides new insights into host-symbiont interactions in psyllids and highlights the importance of host biology and geography in shaping microbiome structure.
Assuntos
Hemípteros , Microbiota , Pyrus , Humanos , Animais , Hemípteros/microbiologia , RNA Ribossômico 16S/genética , Simbiose , Enterobacteriaceae/genética , Insetos , Microbiota/genéticaRESUMO
Phytoplasmas are obligatory intracellular bacteria that colonize the phloem of many plant species and cause hundreds of plant diseases worldwide. In nature, phytoplasmas are primarily transmitted by hemipteran vectors. While all phloem-feeding insects could in principle transmit phytoplasmas, only a limited number of species have been confirmed as vectors. Knowledge about factors that might determine the vector capacity is currently scarce. Here, we characterized the microbiomes of vector and non-vector species of apple proliferation (AP) phytoplasma 'Candidatus Phytoplasma mali' to investigate their potential role in the vector capacity of the host. We performed high-throughput 16S rRNA metabarcoding of the two principal AP-vectors Cacopsylla picta and Cacopsylla melanoneura and eight Cacopsylla species, which are not AP-vectors but co-occur in apple orchards. The microbiomes of all species are dominated by Carsonella, the primary endosymbiont of psyllids and a second uncharacterized Enterobacteriaceae endosymbiont. Each Cacopsylla species harboured a species-specific phylotype of both symbionts. Moreover, we investigated differences between the microbiomes of AP-vector versus non-vector species and identified the predominant endosymbionts but also Wolbachia and several minor taxa as potential indicator species. Our study highlights the importance of considering the microbiome in future investigations of potential factors influencing host vector competence. We investigated the potential role of symbiotic bacteria in the acquisition and transmission of phytoplasma. By comparing the two main psyillid vector species of Apple proliferation (AP) phytoplasma and eight co-occurring species, which are not able to vector AP-phytoplasma, we found differences in the microbial communities of AP-vector and non-vector species, which appear to be driven by the predominant symbionts in both vector species and Wolbachia and several minor taxa in the non-vector species. In contrast, infection with AP-phytoplasma did not affect microbiome composition in both vector species. Our study provides new insights into the endosymbiont diversity of Cacopsylla spp. and highlights the importance of considering the microbiome when investigating potential factors influencing host vector competence.
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Hemípteros , Malus , Microbiota , Phytoplasma , Animais , Hemípteros/microbiologia , Malus/microbiologia , Microbiota/genética , Phytoplasma/genética , Doenças das Plantas/microbiologia , RNA Ribossômico 16S/genéticaRESUMO
The high vector competence of mosquitoes is intrinsically linked to their reproductive strategy because females need a vertebrate blood meal to develop large batches of eggs. However, the molecular mechanisms and pathways regulating mosquito host-seeking behaviour are largely unknown. Here, we test whether host-seeking behaviour may be linked to the female's energy reserves, with low energy levels triggering the search for a nutrient-rich blood meal. Our results demonstrate that sugar feeding delays host-seeking behaviour in the invasive tiger mosquito Aedes albopictus, but the levels of energy reserves do not correlate with changes in host-seeking behaviour. Using tissue-specific gene expression analyses, we show for the first time, to our knowledge, that sugar feeding alone induces a transient up-regulation of several vitellogenesis-related genes in the female fat body, resembling the transcriptional response after a blood meal. Specifically, high expression levels of a vitellogenin gene (Vg-2) correlated with the lowest host-seeking activity of sugar-fed females. Knocking down the Vg-2 gene via RNA interference (RNAi) restored host-seeking behaviour in these females, firmly establishing that Vg-2 gene expression has a pivotal role in regulating host-seeking behaviour in young Ae. albopictus females. The identification of a molecular mechanism regulating host-seeking behaviour in mosquitoes could pave the way for novel vector control strategies aiming to reduce the biting activity of mosquitoes. From an evolutionary perspective, this is the first demonstration of vitellogenin genes controlling feeding-related behaviours in nonsocial insects, while vitellogenins are known to regulate caste-specific foraging and brood-care behaviours in eusocial insects. Hence, this work confirms the key role of vitellogenin in controlling feeding-related behaviours in distantly related insect orders, suggesting that this function could be more ubiquitous than previously thought.
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Aedes/fisiologia , Corpo Adiposo/metabolismo , Comportamento de Busca por Hospedeiro , Vitelogeninas/metabolismo , Aedes/efeitos dos fármacos , Animais , Metabolismo Energético/efeitos dos fármacos , Corpo Adiposo/efeitos dos fármacos , Comportamento Alimentar/efeitos dos fármacos , Feminino , Especificidade de Órgãos/efeitos dos fármacos , Filogenia , Sacarose/farmacologiaRESUMO
Vertical transmission mode is predicted to decrease the virulence of symbionts. However, Wolbachia, a widespread vertically transmitted endosymbiont, exhibits both negative and beneficial effects on arthropod fitness. This 'Jekyll and Hyde' behaviour, as well as its ability to live transiently outside host cells and to establish new infections via horizontal transmission, may reflect the capacity of Wolbachia to exhibit various phenotypes depending on the prevailing environmental constraints. To study the ability of Wolbachia to readily cope with new constraints, we forced this endosymbiont to spread only via horizontal transmission. To achieve this, we performed serial horizontal transfers of haemolymph from Wolbachia-infected to naive individuals of the isopod Armadillidium vulgare. Across passages, we observed phenotypic changes in the symbiotic relationship: (i) The Wolbachia titre increased in both haemolymph and nerve cord but remained stable in ovaries; (ii) Wolbachia infection was benign at the beginning of the experiment, but highly virulent, killing most hosts after only a few passages. Such a phenotypic shift after recurrent horizontal passages demonstrates that Wolbachia can rapidly change its virulence when facing new environmental constraints. We thoroughly discuss the potential mechanism(s) underlying this phenotypic change, which are likely to be crucial for the ongoing radiation of Wolbachia in arthropods.
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Isópodes/microbiologia , Simbiose , Wolbachia/patogenicidade , Animais , Transmissão de Doença Infecciosa , Fenótipo , Virulência , Wolbachia/genéticaRESUMO
The Wolbachia are intracellular endosymbionts widely distributed among invertebrates. These primarily vertically transmitted α-proteobacteria have been intensively studied during the last decades because of their intriguing interactions with hosts, ranging from reproductive manipulations to mutualism. To optimize their vertical transmission from mother to offspring, the Wolbachia have developed fine-tuned strategies. However, the Wolbachia are not restricted to the female gonads and frequently exhibit wide intra-host distributions. This extensive colonization of somatic organs might be necessary for Wolbachia to develop their diverse extended phenotypes. From an endosymbiont's perspective, the within-host environment potentially presents different environmental constraints. Hence, the Wolbachia have to face different intracellular habitats, their host's immune system as well as other microorganisms co-occurring in the same host individual and sometimes even in the same cell. A means for the Wolbachia to protect themselves from these environmental constraints may be to live 'hidden' in vacuoles within host cells. In this review, we summarize the current knowledge regarding the extent of the Wolbachia pandemic and discuss the various environmental constraints these bacteria may have to face within their 'host ecosystem'. Finally, we identify new avenues for future research to better understand the complexity of Wolbachia's interactions with their intracellular environment.
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Artrópodes/microbiologia , Nematoides/microbiologia , Simbiose , Wolbachia/fisiologia , Animais , Artrópodes/genética , Artrópodes/imunologia , Ecossistema , Meio Ambiente , Feminino , Gônadas/microbiologia , Interações Microbianas , Nematoides/genética , Nematoides/imunologia , Fenótipo , Wolbachia/crescimento & desenvolvimentoRESUMO
Some bacteria (notably the genera Bacillus and Clostridium) have the capacity to form endospores that can survive for millions of years in isolated habitats. The genomes of such ancient bacteria provide unique opportunities to understand bacterial evolution and metabolic capabilities over longer time scales. Herein, we sequenced the genome of a 2000-year-old bacterial strain (Mal05) isolated from intact apple seeds recovered during archaeological excavations of a Roman villa in Italy. Phylogenomic analyses revealed that this strain belongs to the species Bacillus stercoris and that it is placed in an early-branching position compared to most other strains of this species. Similar to other Bacillus species, B. stercoris Mal05 had been previously shown to possess antifungal activity. Its genome encodes all the genes necessary for the biosynthesis of fengycin and surfactin, two cyclic lipopeptides known to play a role in the competition of Bacilli with other microorganisms due to their antimicrobial activity. Comparative genomics and analyses of selective pressure demonstrate that these genes are present in all sequenced B. stercoris strains, despite the fact that they are not under strong purifying selection. Hence, these genes may not be essential for the fitness of these bacteria, but they can still provide a competitive advantage against other microorganisms present in the same environment.
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Phytoplasmas are bacterial pathogens located in the plant's phloem that are responsible for several plant diseases and are mainly transmitted by phloem-sucking insects. Apple proliferation (AP) is an economically important disease associated with the presence of 'Candidatus Phytoplasma mali' which is transmitted by two psyllid species. While Cacopsylla picta is a vector in different regions, the vector efficiency of C. melanoneura varies between different populations. This species is considered the main AP vector in Northwestern Italy but plays a minor role in Northeastern Italy and other European regions. To investigate whether the psyllid and/or the phytoplasma subtype drive the phytoplasma acquisition in C. melanoneura, a phytoplasma acquisition experiment was set up using single mating couples of overwintered individuals from different psyllid populations and phytoplasma subtypes. All analyzed insect populations acquired phytoplasma, but with different efficiencies and concentrations. The main factors driving the acquisition were the phytoplasma subtype and its concentration in the leaves of the infected trees together with the psyllid lineage. The phytoplasma concentration in the psyllids was again influenced by the phytoplasma subtype, the psyllid lineage and the region of origin, whereas the phytoplasma concentration in the leaves and the psyllid haplotype defined with the cytochrome oxidase I gene had only a minor impact on the phytoplasma concentration. This is the first study evaluating the roles of both the psyllid haplotype and the phytoplasma subtype on the acquisition process and highlights the importance of C. melanoneura as an additional AP vector. Supplementary Information: The online version contains supplementary material available at 10.1007/s10340-023-01699-1.
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The order Holosporales (Alphaproteobacteria) encompasses obligate intracellular bacterial symbionts of diverse Eukaryotes. These bacteria have highly streamlined genomes and can have negative fitness effects on the host. Herein, we present a comparative analysis of the first genome sequences of 'Ca. Hepatincola porcellionum', a facultative symbiont occurring extracellularly in the midgut glands of terrestrial isopods. Using a combination of long-read and short-read sequencing, we obtained the complete circular genomes of two Hepatincola strains and an additional metagenome-assembled draft genome. Phylogenomic analysis validated its phylogenetic position as an early-branching family-level clade relative to all other established Holosporales families associated with protists. A 16S rRNA gene survey revealed that this new family encompasses diverse bacteria associated with both marine and terrestrial host species, which expands the host range of Holosporales bacteria from protists to several phyla of the Ecdysozoa (Arthropoda and Priapulida). Hepatincola has a highly streamlined genome with reduced metabolic and biosynthetic capacities as well as a large repertoire of transmembrane transporters. This suggests that this symbiont is rather a nutrient scavenger than a nutrient provider for the host, likely benefitting from a nutrient-rich environment to import all necessary metabolites and precursors. Hepatincola further possesses a different set of bacterial secretion systems compared to protist-associated Holosporales, suggesting different host-symbiont interactions depending on the host organism.
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IMPORTANCE: Heritable beneficial bacterial endosymbionts have been crucial for the evolutionary success of numerous insects by enabling the exploitation of nutritionally limited food sources. Herein, we describe a previously unknown dual endosymbiosis in the psyllid genus Cacopsylla, consisting of the primary endosymbiont "Candidatus Carsonella ruddii" and a co-occurring Enterobacteriaceae bacterium for which we propose the name "Candidatus Psyllophila symbiotica." Its localization within the bacteriome and its small genome size confirm that Psyllophila is a co-primary endosymbiont widespread within the genus Cacopsylla. Despite its highly eroded genome, Psyllophila perfectly complements the tryptophan biosynthesis pathway that is incomplete in the co-occurring Carsonella. Moreover, the genome of Psyllophila is almost as small as Carsonella's, suggesting an ancient dual endosymbiosis that has now reached a precarious stage where any additional gene loss would make the system collapse. Hence, our results shed light on the dynamic interactions of psyllids and their endosymbionts over evolutionary time.
Assuntos
Hemípteros , Animais , Hemípteros/genética , Simbiose/genética , Filogenia , Bactérias , Enterobacteriaceae/genéticaRESUMO
Most sap-feeding insects maintain obligate relationships with endosymbiotic bacteria that provide their hosts with essential nutrients. However, knowledge about the dynamics of endosymbiont titers across seasons in natural host populations is scarce. Here, we used quantitative PCR to investigate the seasonal dynamics of the dual endosymbionts "Candidatus Carsonella ruddii" and "Ca. Psyllophila symbiotica" in a natural population of the pear psyllid Cacopsylla pyricola (Hemiptera: Psylloidea: Psyllidae). Psyllid individuals were collected across an entire year, covering both summer and overwintering generations. Immatures harboured the highest titers of both endosymbionts, while the lowest endosymbiont density was observed in males. The density of Carsonella remained high and relatively stable across the vegetative period of the pear trees, but significantly dropped during the non-vegetative period, overlapping with C. pyricola's reproductive diapause. In contrast, the titer of Psyllophila was consistently higher than Carsonella's and exhibited fluctuations throughout the sampling year, which might be related to host age. Despite a tightly integrated metabolic complementarity between Carsonella and Psyllophila, our findings highlight differences in their density dynamics throughout the year, that might be linked to their metabolic roles at different life stages of the host.
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Hemípteros , Pyrus , Humanos , Masculino , Animais , Estações do Ano , Hemípteros/microbiologia , Simbiose , BactériasRESUMO
Changes in agricultural land-use of saltmarshes along the German North Sea coast have favoured the succession of the marsh grass Elytrigia atherica over the long-established Spartina anglica. Consequently, E. atherica represents a potential food source of increasing importance for plant-feeding soil detritivores. Considering the importance of this ecological guild for decomposition processes and nutrient cycling, we focussed on two sympatric saltmarsh soil macrodetritivores and their associated gut microbiota to investigate how the digestive processes of these species may be affected by changing plant food sources. Using genetic fingerprints of partial 16S rRNA gene sequences, we analysed composition and diversity of the bacterial gut community in a diplopod and an amphipod crustacean in relation to different feeding regimes representing the natural vegetation changes. Effects of syntopy on the host-specific gut microbiota were also taken into account by feeding the two detritivore species either independently or on the same plant sample. Bacterial community composition was influenced by both the host species and the available plant food sources, but the latter had a stronger effect on microbial community structure. Furthermore, bacterial diversity was highest after feeding on a mixture of both plant species, regardless of the host species. The gut microbiota of these two detritivores can thus be expected to change along with the on-going succession at the plant community level in this environment. Cloning and sequencing of bacterial 16S rRNA gene fragments further indicated a host-related effect since the two detritivores differed in terms of predominant bacterial taxa: diplopods harboured mainly representatives of the phyla Bacteroidetes and Gammaproteobacteria. In contrast, the genus Vibrio was found for the amphipod host across all feeding conditions.
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Anfípodes/fisiologia , Artrópodes/fisiologia , Bactérias/genética , Comportamento Alimentar , Trato Gastrointestinal/microbiologia , Poaceae/classificação , Áreas Alagadas , Anfípodes/microbiologia , Animais , Artrópodes/microbiologia , Bactérias/classificação , Bactérias/isolamento & purificação , Bacteroides/genética , Bacteroides/isolamento & purificação , Comportamento Animal , Ecossistema , Gammaproteobacteria/genética , Gammaproteobacteria/isolamento & purificação , Metagenoma , Dados de Sequência Molecular , RNA Ribossômico 16S/genética , Análise de Sequência de DNA , Vibrio/genética , Vibrio/isolamento & purificaçãoRESUMO
Wolbachia is one of the most abundant intracellular symbionts of arthropods and has profound effects on host biology. Wolbachia transmission and host phenotypes often depend on its density within the host, which can be affected by multiple biotic and abiotic factors. However, very few studies measured Wolbachia density in natural host populations. Here, we describe Wolbachia in the pear psyllid Cacopsylla pyri from three populations in the Czech Republic. Using phylogenetic analyses based on wsp and multilocus sequence typing genes, we demonstrate that C. pyri harbours three new Wolbachia strains from supergroup B. A fourth Wolbachia strain from supergroup A was also detected in parasitised immatures of C. pyri, but likely came from a hymenopteran parasitoid. To obtain insights into natural Wolbachia infection dynamics, we quantified Wolbachia in psyllid individuals from the locality with the highest prevalence across an entire year, spanning several seasonal generations of the host. All tested females were infected and Wolbachia density remained stable across the entire period, suggesting a highly efficient vertical transmission and little influence from the environment and different host generations. In contrast, we observed a tendency towards reduced Wolbachia density in males which may suggest sex-related differences in Wolbachia-psyllid interactions.
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Hemípteros , Pyrus , Wolbachia , Animais , Feminino , Hemípteros/genética , Masculino , Filogenia , Estações do Ano , Wolbachia/genéticaRESUMO
While parasites are likely to encounter several potential intermediate hosts in natural communities, a parasite's actual range of compatible hosts is limited by numerous biological factors ranging from behaviour to immunology. In crustaceans, two major components of immunity are haemocytes and the prophenoloxidase system involved in the melanisation of foreign particles. Here, we analysed metazoan parasite prevalence and loads in the two sympatric crab species Hemigrapsus crenulatus and Macrophthalmus hirtipes at two sites. In parallel, we analysed the variation in haemocyte concentration and amount of circulating phenoloxidase (PO) in the haemolymph of the same individuals in an attempt to (a) explain differences in parasite prevalence and loads in the two species at two sites and (b) assess the impact of parasites on these immune parameters. M. hirtipes harboured more parasites but also exhibited higher haemocyte concentrations than H. crenulatus independent of the study site. Thus, higher investment in haemocyte production for M. hirtipes does not seem to result in higher resistance to parasites. Analyses of variation in immune parameters for the two crab species between the two sites that differed in parasite prevalence showed common trends. (a) In general, haemocyte concentrations were higher at the site experiencing higher parasitic pressure while circulating PO activity was lower and (b) haemocyte concentrations were influenced by microphallid trematode metacercariae in individuals from the site with higher parasitic pressure. We suggest that the higher haemocyte concentrations observed in both crab species exposed to higher parasitic pressure may represent an adaptive response to the impact of parasites on this immune parameter.
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Braquiúros/imunologia , Braquiúros/parasitologia , Carga Parasitária , Parasitos/imunologia , Parasitos/isolamento & purificação , Animais , Feminino , Hemócitos/imunologia , Hemolinfa/química , Hemolinfa/citologia , Hemolinfa/imunologia , Masculino , Monofenol Mono-Oxigenase/análise , Monofenol Mono-Oxigenase/imunologia , Nova Zelândia , PrevalênciaRESUMO
BACKGROUND: The life cycles of many insect species include an obligatory or facultative diapause stage with arrested development and low metabolic activity as an overwintering strategy. Diapause is characterised by profound physiological changes in endocrine activity, cell proliferation and nutrient metabolism. However, little is known regarding host-microbiome interactions during diapause, despite the importance of bacterial symbionts for host nutrition and development. In this work, we investigated (i) the role of the microbiome for host nutrient allocation during diapause and (ii) the impact of larval diapause on microbiome dynamics in the parasitoid wasp Nasonia vitripennis, a model organism for host-microbiome interactions. RESULTS: Our results demonstrate that the microbiome is essential for host nutrient allocation during diapause in N. vitripennis, as axenic diapausing larvae had consistently lower glucose and glycerol levels than conventional diapausing larvae, especially when exposed to cold temperature. In turn, microbiome composition was altered in diapausing larvae, potentially due to changes in the surrounding temperature, host nutrient levels and a downregulation of host immune genes. Importantly, prolonged larval diapause had a transstadial effect on the adult microbiome, with unknown consequences for host fitness. Notably, the most dominant microbiome member, Providencia sp., was drastically reduced in adults after more than 4 months of larval diapause, while potential bacterial pathogens increased in abundance. CONCLUSION: This work investigates host-microbiome interactions during a crucial developmental stage, which challenges both the insect host and its microbial associates. The impact of diapause on the microbiome is likely due to several factors, including altered host regulatory mechanisms and changes in the host environment. Video Abstract.
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Diapausa , Microbiota , Vespas , Animais , Temperatura Baixa , LarvaRESUMO
The genus Arsenophonus represents one of the most widespread clades of insect endosymbionts, including reproductive manipulators and bacteriocyte-associated primary endosymbionts. Two strains belonging to the Arsenophonus clade have been identified as insect-vectored plant pathogens of strawberry and sugar beet. The bacteria accumulate in the phloem of infected plants, ultimately causing leaf yellows and necrosis. These symbionts therefore represent excellent model systems to investigate the evolutionary transition from a purely insect-associated endosymbiont towards an insect-vectored phytopathogen. Using quantitative PCR and transmission electron microscopy, we demonstrate that 'Candidatus Phlomobacter fragariae', bacterial symbiont of the planthopper Cixius wagneri and the causative agent of Strawberry Marginal Chlorosis disease, can be transmitted from an infected strawberry plant to multiple daughter plants through stolons. Stolons are horizontally growing stems enabling the nutrient provisioning of daughter plants during their early growth phase. Our results show that Phlomobacter was abundant in the phloem sieve elements of stolons and was efficiently transmitted to daughter plants, which rapidly developed disease symptoms. From an evolutionary perspective, Phlomobacter is, therefore, not only able to survive within the plant after transmission by the insect vector, but can even be transmitted to new plant generations, independently from its ancestral insect host.
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One of the most difficult experimental challenges today is testing the evolutionary dynamics shaping complex host-microbiome interactions. We investigated host-microbiome codiversification in response to xenobiotic-induced selection using an experimental evolution approach. To this end, we exposed the parasitoid wasp Nasonia vitripennis to sublethal concentrations of the widely used herbicide atrazine for 85 generations. Our results reveal that atrazine exposure not only mediated adaptive changes within the microbiome, which conferred host resistance to atrazine toxicity, but also exerted selective pressure on the host genome and altered host gene expression and immune response. Furthermore, microbiome transplant experiments reveal a decreased survival of adults from the control population after exposure to the evolved microbiome of the atrazine-exposed population, while no such decrease occurred in the reciprocal transplant. These results indicate that xenobiotic-induced selection mediated host-microbiome coadaptation, ultimately leading to a new host genome-microbiome equilibrium.
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Mosquitoes are important vectors of human pathogens, which are transmitted by female mosquitoes via blood-feeding. Larval nutrition can have an important impact on the number of blood meals taken by adult females shortly after emergence, as nutritional deficiencies during the larval stage may result in pre-vitellogenic blood meals, which are not invested into egg development but into the endogenous nutrient reserves of the female. Here, we investigated the impact of nutrient deprivation during the larval stage on adult nutrient metabolism, longevity and blood-seeking behaviour in females of the invasive Asian tiger mosquito Aedes albopictus. We demonstrate that Ae. albopictus females are able to compensate for nutrient deprivation during the larval stage by increasing their development time until sufficient nutrients are acquired. Nonetheless, nutrient-poor larval conditions had a long-lasting priming effect on adult female metabolism, since these females accumulated lower nutrient reserves from carbohydrates and survived longer compared to females reared in nutrient-rich larval conditions. Moreover, nutrient and ATP levels of females from nutrient-poor larval conditions remained stable over a longer timespan without access to additional carbohydrates. This suggests differences in adult female metabolism in response to larval nutrition, with potential impact on the vectorial capacity of female mosquitoes.
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Aedes/fisiologia , Fenômenos Fisiológicos da Nutrição Animal , Mosquitos Vetores/fisiologia , Aedes/crescimento & desenvolvimento , Animais , Comportamento Alimentar , Feminino , Larva/crescimento & desenvolvimento , Larva/fisiologia , Longevidade , Mosquitos Vetores/crescimento & desenvolvimentoRESUMO
Wolbachia are widespread heritable endosymbionts of arthropods notorious for their profound effects on host fitness as well as for providing protection against viruses and eukaryotic parasites, indicating that they can interact with other microorganisms sharing the same host environment. Using the terrestrial isopod crustacean Armadillidium vulgare, its highly diverse microbiota (>200 bacterial genera) and its three feminizing Wolbachia strains (wVulC, wVulM, wVulP) as a model system, the present study demonstrates that Wolbachia can even influence the composition of a diverse bacterial community under both laboratory and natural conditions. While host origin is the major determinant of the taxonomic composition of the microbiota in A. vulgare, Wolbachia infection affected both the presence and, more importantly, the abundance of many bacterial taxa within each host population, possibly due to competitive interactions. Moreover, different Wolbachia strains had different impacts on microbiota composition. As such, infection with wVulC affected a higher number of taxa than infection with wVulM, possibly due to intrinsic differences in virulence and titer between these two strains. In conclusion, this study shows that heritable endosymbionts such as Wolbachia can act as biotic factors shaping the microbiota of arthropods, with as yet unknown consequences on host fitness.
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Estruturas Animais/microbiologia , Isópodes/microbiologia , Microbiota , Wolbachia/crescimento & desenvolvimento , Animais , Bactérias/classificação , Bactérias/genética , Metagenômica , Interações MicrobianasRESUMO
BACKGROUND: Woodlice are recognized as keystone species in terrestrial ecosystems due to their role in the decomposition of organic matter. Thus, they contribute to lignocellulose degradation and nutrient cycling in the environment together with other macroarthropods. Lignocellulose is the main component of plants and is composed of cellulose, lignin and hemicellulose. Its digestion requires the action of multiple Carbohydrate-Active enZymes (called CAZymes), typically acting together as a cocktail with complementary, synergistic activities and modes of action. Some invertebrates express a few endogenous lignocellulose-degrading enzymes but in most species, an efficient degradation and digestion of lignocellulose can only be achieved through mutualistic associations with endosymbionts. Similar to termites, it has been suspected that several bacterial symbionts may be involved in lignocellulose degradation in terrestrial isopods, by completing the CAZyme repertoire of their hosts. RESULTS: To test this hypothesis, host transcriptomic and microbiome shotgun metagenomic datasets were obtained and investigated from the pill bug Armadillidium vulgare. Many genes of bacterial and archaeal origin coding for CAZymes were identified in the metagenomes of several host tissues and the gut content of specimens from both laboratory lineages and a natural population of A. vulgare. Some of them may be involved in the degradation of cellulose, hemicellulose, and lignin. Reconstructing a lignocellulose-degrading microbial community based on the prokaryotic taxa contributing relevant CAZymes revealed two taxonomically distinct but functionally redundant microbial communities depending on host origin. In parallel, endogenous CAZymes were identified from the transcriptome of the host and their expression in digestive tissues was demonstrated by RT-qPCR, demonstrating a complementary enzyme repertoire for lignocellulose degradation from both the host and the microbiome in A. vulgare. CONCLUSIONS: Our results provide new insights into the role of the microbiome in the evolution of terrestrial isopods and their adaptive radiation in terrestrial habitats.