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1.
J Invertebr Pathol ; 199: 107947, 2023 07.
Artigo em Inglês | MEDLINE | ID: mdl-37285901

RESUMO

Heritable microbes that exhibit reproductive parasitism are common in insects. One class of these are the male-killing bacteria, which are found in a broad range of insect hosts. Commonly, our knowledge of the incidence of these microbes is based on one or a few sampling sites, and the degree and causes of spatial variation are unclear. In this paper, we examine the incidence of the son-killer microbe Arsenophonus nasoniae across European populations of its wasp host, Nasonia vitripennis. In preliminary work, we noticed two female N. vitripennis producing highly female biased sex ratios in a field study from the Netherlands and Germany. When tested, the brood from Germany was revealed to be infected with A. nasoniae. We then completed a broad survey in 2012, in which fly pupal hosts of N. vitripennis were collected from vacated birds' nests from four European populations, N. vitripennis wasps allowed to emerge and then tested for A. nasoniae presence through PCR assay. We then developed a new screening methodology based on direct PCR assays of fly pupae and applied this to ethanol-preserved material collected from great tit (Parus major) nests in Portugal. These data show A. nasoniae is found widely in European N. vitripennis, being present in Germany, the UK, Finland, Switzerland and Portugal. Samples varied in the frequency with which they carry A. nasoniae, from being rare to being present in 50% of the pupae parasitised by N. vitripennis. Direct screening of ethanol-preserved fly pupae was an effective method for revealing both wasp and A. nasoniae infection, and will facilitate sample transport across national boundaries. Future research should examine the causes of variation in frequency, in particular testing the hypothesis that N. vitripennis superparasitism rates drive the variation in A. nasoniae frequency through providing opportunities for infectious transmission.


Assuntos
Gammaproteobacteria , Vespas , Feminino , Masculino , Animais , Vespas/microbiologia , Núcleo Familiar , Enterobacteriaceae , Insetos , Europa (Continente)
2.
Artigo em Inglês | MEDLINE | ID: mdl-35930469

RESUMO

The genus Arsenophonus has been traditionally considered to comprise heritable bacterial symbionts of arthropods. Recent work has reported a microbe related to the type species Arsenophonus nasoniae as infecting the honey bee, Apis mellifera. The association was unusual for members of the genus in that the microbe-host interaction arose through environmental and social exposure rather than vertical transmission. In this study, we describe the in vitro culture of ArsBeeUST, a strain of this microbe isolated from A. mellifera in the USA. The 16S rRNA sequence of the isolated strain indicates it falls within the genus Arsenophonus. Biolog analysis indicates the bacterium has a restricted range of nutrients that support growth. In vivo experiments demonstrate the strain proliferates rapidly on injection into A. mellifera hosts. We further report the closed genome sequence for the strain. The genome is 3.3 Mb and the G+C content is 37.6 mol%, which is smaller than A. nasoniae but larger than the genomes reported for non-culturable Arsenophonus symbionts. The genome is complex, with six extrachromosomal elements and 11 predicted intact phage elements, but notably less complex than A. nasoniae. Strain ArsBeeUST is clearly distinct from the type species A. nasoniae on the basis of genome sequence, with 92 % average nucleotide identity. Based on our results, we propose Arsenophonus apicola sp. nov., with the type strain ArsBeeUST (CECT 30499T=DSM113403T=LMG 32504T).


Assuntos
Ácidos Graxos , Simbiose , Animais , Bactérias/genética , Técnicas de Tipagem Bacteriana , Composição de Bases , Abelhas , DNA Bacteriano/genética , Ácidos Graxos/química , Filogenia , RNA Ribossômico 16S/genética , Análise de Sequência de DNA , Simbiose/genética
3.
ISME J ; 15(10): 2956-2968, 2021 10.
Artigo em Inglês | MEDLINE | ID: mdl-33941888

RESUMO

A dynamic continuum exists from free-living environmental microbes to strict host-associated symbionts that are vertically inherited. However, knowledge of the forces that drive transitions in symbiotic lifestyle and transmission mode is lacking. Arsenophonus is a diverse clade of bacterial symbionts, comprising reproductive parasites to coevolving obligate mutualists, in which the predominant mode of transmission is vertical. We describe a symbiosis between a member of the genus Arsenophonus and the Western honey bee. The symbiont shares common genomic and predicted metabolic properties with the male-killing symbiont Arsenophonus nasoniae, however we present multiple lines of evidence that the bee Arsenophonus deviates from a heritable model of transmission. Field sampling uncovered spatial and seasonal dynamics in symbiont prevalence, and rapid infection loss events were observed in field colonies and laboratory individuals. Fluorescent in situ hybridisation showed Arsenophonus localised in the gut, and detection was rare in screens of early honey bee life stages. We directly show horizontal transmission of Arsenophonus between bees under varying social conditions. We conclude that honey bees acquire Arsenophonus through a combination of environmental exposure and social contacts. These findings uncover a key link in the Arsenophonus clades trajectory from free-living ancestral life to obligate mutualism, and provide a foundation for studying transitions in symbiotic lifestyle.


Assuntos
Gammaproteobacteria , Simbiose , Animais , Bactérias/genética , Abelhas , Enterobacteriaceae , Masculino , Filogenia
4.
mBio ; 11(2)2020 03 24.
Artigo em Inglês | MEDLINE | ID: mdl-32209690

RESUMO

Mobile elements-plasmids and phages-are important components of microbial function and evolution via traits that they encode and their capacity to shuttle genetic material between species. We here report the unusually rich array of mobile elements within the genome of Arsenophonus nasoniae, the son-killer symbiont of the parasitic wasp Nasonia vitripennis This microbe's genome has the highest prophage complement reported to date, with over 50 genomic regions that represent either intact or degraded phage material. Moreover, the genome is predicted to include 17 extrachromosomal genetic elements, which carry many genes predicted to be important at the microbe-host interface, derived from a diverse assemblage of insect-associated gammaproteobacteria. In our system, this diversity was previously masked by repetitive mobile elements that broke the assembly derived from short reads. These findings suggest that other complex bacterial genomes will be revealed in the era of long-read sequencing.IMPORTANCE The biology of many bacteria is critically dependent on genes carried on plasmid and phage mobile elements. These elements shuttle between microbial species, thus providing an important source of biological innovation across taxa. It has recently been recognized that mobile elements are also important in symbiotic bacteria, which form long-lasting interactions with their host. In this study, we report a bacterial symbiont genome that carries a highly complex array of these elements. Arsenophonus nasoniae is the son-killer microbe of the parasitic wasp Nasonia vitripennis and exists with the wasp throughout its life cycle. We completed its genome with the aid of recently developed long-read technology. This assembly contained over 50 chromosomal regions of phage origin and 17 extrachromosomal elements within the genome, encoding many important traits at the host-microbe interface. Thus, the biology of this symbiont is enabled by a complex array of mobile elements.


Assuntos
Gammaproteobacteria/genética , Transferência Genética Horizontal , Genoma Bacteriano , Sequências Repetitivas Dispersas , Simbiose/genética , Vespas/microbiologia , Animais , Bacteriófagos/genética , Genômica , Filogenia , Sequências Repetitivas de Ácido Nucleico
5.
Environ Microbiol ; 21(8): 3172-3182, 2019 08.
Artigo em Inglês | MEDLINE | ID: mdl-31237728

RESUMO

Maternally heritable symbionts are common in arthropods and represent important partners and antagonists. A major impediment to understanding the mechanistic basis of these symbioses has been lack of genetic manipulation tools, for instance, those enabling transgenic GFP expression systems for in vivo visualization. Here, we transform the 'son-killer' reproductive parasite Arsenophonus nasoniae that infects the parasitic wasp Nasonia vitripennis with the plasmid pOM1-gfp, re-introduce this strain to N. vitripennis and then used this system to track symbiont life history in vivo. These data revealed transfer of the symbiont into the fly pupa by N. vitripennis during oviposition and N. vitripennis larvae developing infection over time through feeding. A strong tropism of A. nasoniae to the N. vitripennis ovipositor developed during wasp pupation, which aids onward transmission. The symbiont was also visualized in diapause larvae. Occasional necrotic diapause larvae were observed which displayed intense systemic infection alongside widespread melanotic nodules indicative of an active but failed immune response. Our results provide the foundation for the study of this symbiosis through in vivo tracking of the fate of symbionts through host development, which is rarely achieved in heritable microbe/insect interactions.


Assuntos
Gammaproteobacteria/metabolismo , Vespas/microbiologia , Animais , Feminino , Gammaproteobacteria/genética , Insetos , Larva , Pupa , Simbiose/genética , Tropismo
6.
Oncotarget ; 8(26): 42382-42397, 2017 Jun 27.
Artigo em Inglês | MEDLINE | ID: mdl-28415575

RESUMO

Many potassium channel families are over-expressed in cancer, but their mechanistic role in disease progression is poorly understood. Potassium channels modulate membrane potential (Vmem) and thereby influence calcium ion dynamics and other voltage-sensitive signaling mechanisms, potentially acting as transcriptional regulators. This study investigated the differential response to over-expression and activation of a cancer-associated potassium channel, the intermediate conductance calcium-activated potassium channel (IK), on aggressive behaviors in mammary epithelial and breast cancer cell lines. IK was over-expressed in the highly metastatic breast cancer cell line MDA-MB-231 and the spontaneously immortalized breast epithelial cell line MCF-10A, and the effect on cancer-associated behaviors was assessed. IK over-expression increased primary tumor growth and metastasis of MDA-MB-231 in orthotopic xenografts, demonstrating for the first time in any cancer type that increased IK is sufficient to promote cancer aggression. The primary tumors had similar vascularization as determined by CD31 staining and similar histological characteristics. Interestingly, despite the increased in vivo growth and metastasis, neither IK over-expression nor activation with agonist had a significant effect on MDA-MB-231 proliferation, invasion, or migration in vitro. In contrast, IK decreased MCF-10A proliferation and invasion through Matrigel but had no effect on migration in a scratch-wound assay. We conclude that IK activity is sufficient to promote cell aggression in vivo. Our data provide novel evidence supporting IK and downstream signaling networks as potential targets for cancer therapies.


Assuntos
Ativação do Canal Iônico , Canais de Potássio/metabolismo , Animais , Neoplasias da Mama/metabolismo , Neoplasias da Mama/patologia , Linhagem Celular Tumoral , Movimento Celular/genética , Proliferação de Células , Modelos Animais de Doenças , Feminino , Pontos de Checagem da Fase G2 do Ciclo Celular/genética , Expressão Gênica , Xenoenxertos , Humanos , Potenciais da Membrana , Camundongos , Camundongos Knockout , Canais de Potássio/agonistas , Canais de Potássio/genética , Ensaio Tumoral de Célula-Tronco
7.
PLoS Pathog ; 12(6): e1005629, 2016 Jun.
Artigo em Inglês | MEDLINE | ID: mdl-27322651

RESUMO

Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont's spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that 'reproductive parasite' phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections.


Assuntos
Transmissão de Doença Infecciosa/veterinária , Proteobactérias/patogenicidade , Simbiose/fisiologia , Vespas/parasitologia , Animais , Feminino , Masculino , Razão de Masculinidade
8.
ISME J ; 10(8): 1915-24, 2016 08.
Artigo em Inglês | MEDLINE | ID: mdl-26978164

RESUMO

Microbes can defend their host against virulent infections, but direct evidence for the adaptive origin of microbe-mediated protection is lacking. Using experimental evolution of a novel, tripartite interaction, we demonstrate that mildly pathogenic bacteria (Enterococcus faecalis) living in worms (Caenorhabditis elegans) rapidly evolved to defend their animal hosts against infection by a more virulent pathogen (Staphylococcus aureus), crossing the parasitism-mutualism continuum. Host protection evolved in all six, independently selected populations in response to within-host bacterial interactions and without direct selection for host health. Microbe-mediated protection was also effective against a broad spectrum of pathogenic S. aureus isolates. Genomic analysis implied that the mechanistic basis for E. faecalis-mediated protection was through increased production of antimicrobial superoxide, which was confirmed by biochemical assays. Our results indicate that microbes living within a host may make the evolutionary transition to mutualism in response to pathogen attack, and that microbiome evolution warrants consideration as a driver of infection outcome.


Assuntos
Caenorhabditis elegans/microbiologia , Enterococcus faecalis/fisiologia , Staphylococcus aureus/patogenicidade , Simbiose , Animais , Evolução Biológica , Caenorhabditis elegans/genética , Enterococcus faecalis/genética , Feminino , Microbiota
9.
Artigo em Inglês | MEDLINE | ID: mdl-25934011

RESUMO

Most species of insect, and many other plants and animals, carry maternally heritable microorganisms-viruses, bacteria, unicellular eukaryotes, and fungi that pass from a female host to her progeny. Maternal inheritance establishes a correlation between the fitness of symbiont and host female, which can select for the symbiont to contribute to host fitness. Nevertheless, its lack of transmission through male hosts places the symbiont in conflict with biparentally inherited nuclear genes. In this review, we first examine how this conflict is manifest in selection to promote the production and survival of infected female hosts and gametes. We then examine how the distorted population sex ratios that they produce may affect host reproductive ecology, and thus the intensity of other conflicts associated with sexual reproduction. Finally, we examine evolved host responses to symbiont manipulation. We argue that the unusual intensity of symbiont-host conflict generates extreme selection pressures that can drive changes in sex-determination systems, the basic pathway through which males and females are constructed.


Assuntos
Reprodução , Simbiose , Animais , Feminino , Masculino , Razão de Masculinidade
10.
PLoS One ; 9(7): e95122, 2014.
Artigo em Inglês | MEDLINE | ID: mdl-24988478

RESUMO

Symbionts can substantially affect the evolution and ecology of their hosts. The investigation of the tissue-specific distribution of symbionts (tissue tropism) can provide important insight into host-symbiont interactions. Among other things, it can help to discern the importance of specific transmission routes and potential phenotypic effects. The intracellular bacterial symbiont Wolbachia has been described as the greatest ever panzootic, due to the wide array of arthropods that it infects. Being primarily vertically transmitted, it is expected that the transmission of Wolbachia would be enhanced by focusing infection in the reproductive tissues. In social insect hosts, this tropism would logically extend to reproductive rather than sterile castes, since the latter constitute a dead-end for vertically transmission. Here, we show that Wolbachia are not focused on reproductive tissues of eusocial insects, and that non-reproductive tissues of queens and workers of the ant Acromyrmex echinatior, harbour substantial infections. In particular, the comparatively high intensities of Wolbachia in the haemolymph, fat body, and faeces, suggest potential for horizontal transmission via parasitoids and the faecal-oral route, or a role for Wolbachia modulating the immune response of this host. It may be that somatic tissues and castes are not the evolutionary dead-end for Wolbachia that is commonly thought.


Assuntos
Formigas/microbiologia , Interações Hospedeiro-Patógeno/fisiologia , Simbiose , Wolbachia/fisiologia , Animais , Corpo Adiposo/microbiologia , Fezes/microbiologia , Feminino , Células Germinativas/microbiologia , Hemolinfa/microbiologia , Ovário/microbiologia
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