Animal–microbe interactions and the evolution of nervous systems

Eisthen, Heather L.; Theis, Kevin R.

doi:10.1098/rstb.2015.0052

Cited by 28 publications

(16 citation statements)

References 135 publications

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“…A wide variety of microbes have evolved the ability to manipulate animal behavior in ways that appear to advance microbial fitness (Eisthen and Theis, 2016;Forsythe et al, 2012;Hoover et al, 2011;Hughes et al, 2016;Libersat, 2003;Rohrscheib and Brownlie, 2013;Roy et al, 2006;Sampson and Mazmanian, 2015;Wang et al, 2015) . Among them is the fungal pathogen of dipterans Entomophthora muscae .…”

Section: Introductionmentioning

confidence: 99%

Entomophthovirus: An insect-derived iflavirus that infects a behavior manipulating fungal pathogen of dipterans

Bronski

et al. 2018

Preprint

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We discovered a virus infecting Entomophthora muscae , a behavior-manipulating fungal pathogen of dipterans. The virus, which we name Entomophthovirus, is a capsid-forming, positive-strand RNA virus in the viral family iflaviridae, whose known members almost exclusively infect insects. We show that the virus RNA is expressed at high levels in fungal cells in vitro and during in vivo infections of Drosophila melanogaster , and that virus particles are present in E. muscae . Two close relatives of the virus had been previously described as insect viruses based on the presence of viral genomes in transcriptomes assembled from RNA extracted from wild dipterans. By analyzing sequencing data from these earlier reports, we show that both dipteran samples were co-infected with E. muscae . We also find the virus in RNA sequencing data from samples of two other species of dipterans, Musca domestica and Delia radicum , known to be infected with E. muscae . These data establish that Entomophthovirus is widely, and seemingly obligately, associated with E. muscae . As other members of the iflaviridae cause behavioral changes in insects, we speculate on the possibility that Entomophthovirus plays a role in E. muscae involved host manipulation.

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Section: Introductionmentioning

confidence: 99%

Entomophthovirus: An insect-derived iflavirus that infects a behavior manipulating fungal pathogen of dipterans

Bronski

et al. 2018

Preprint

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“…In the following article [22], Eisthen & Theis emphasize the degree to which environmental and symbiotic microbes play a central role in the physiology of the CNS. The suggestion is that such interactions, which today command the attention of biomedical researchers, may have archaic origins to the extent that microbes once played a crucial role in the evolution of neural systems by driving the evolution of epithelial-microbial interactions leading to internalization of specialized conducting cells, which assumed the role of proto-neurons.…”

Section: Organization and Contributions To This Issuementioning

confidence: 99%

Introduction to ‘Homology and convergence in nervous system evolution’

Strausfeld

Hirth

2016

Phil. Trans. R. Soc. B

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The origin of brains and central nervous systems (CNSs) is thought to have occurred before the Palaeozoic era 540 Ma. Yet in the absence of tangible evidence, there has been continued debate whether today's brains and nervous systems derive from one ancestral origin or whether similarities among them are due to convergent evolution. With the advent of molecular developmental genetics and genomics, it has become clear that homology is a concept that applies not only to morphologies, but also to genes, developmental processes, as well as to behaviours. Comparative studies in phyla ranging from annelids and arthropods to mammals are providing evidence that corresponding developmental genetic mechanisms act not only in dorso–ventral and anterior–posterior axis specification but also in segmentation, neurogenesis, axogenesis and eye/photoreceptor cell formation that appear to be conserved throughout the animal kingdom. These data are supported by recent studies which identified Mid-Cambrian fossils with preserved soft body parts that present segmental arrangements in brains typical of modern arthropods, and similarly organized brain centres and circuits across phyla that may reflect genealogical correspondence and control similar behavioural manifestations. Moreover, congruence between genetic and geological fossil records support the notion that by the ‘Cambrian explosion’ arthropods and chordates shared similarities in brain and nervous system organization. However, these similarities are strikingly absent in several sister- and outgroups of arthropods and chordates which raises several questions, foremost among them: what kind of natural laws and mechanisms underlie the convergent evolution of such similarities? And, vice versa: what are the selection pressures and genetic mechanisms underlying the possible loss or reduction of brains and CNSs in multiple lineages during the course of evolution? These questions were addressed at a Royal Society meeting to discuss homology and convergence in nervous system evolution. By integrating knowledge ranging from evolutionary theory and palaeontology to comparative developmental genetics and phylogenomics, the meeting covered disparities in nervous system origins as well as correspondences of neural circuit organization and behaviours, all of which allow evidence-based debates for and against the proposition that the nervous systems and brains of animals might derive from a common ancestor.

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“…Decoding the connection between metabolites, microbes, and the host is yet another exciting frontier in metaorganism research ( Dorrestein et al, 2014 ). This is highly relevant in the light of recent evidence that microbially produced metabolites influence different organ systems, such as microbe-brain connections, bone metabolism, or immune functions ( Cryan and Dinan, 2012 ; Dorrestein et al, 2014 ; Charles et al, 2015 ; Eisthen and Theis, 2016 ). Multi-omics approaches in which the metabolome, the microbiome, and the host immune system are assessed simultaneously are feasible in the Hydra model and will help to decipher this new connection.…”

Section: Hydra and Its Microbiome As An Experimental Modelmentioning

confidence: 99%

Transitioning from Microbiome Composition to Microbial Community Interactions: The Potential of the Metaorganism Hydra as an Experimental Model

Deines

Bosch

2016

Front. Microbiol.

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Animals are home to complex microbial communities, which are shaped through interactions within the community, interactions with the host, and through environmental factors. The advent of high-throughput sequencing methods has led to novel insights in changing patterns of community composition and structure. However, deciphering the different types of interactions among community members, with their hosts and their interplay with their environment is still a challenge of major proportion. The emerging fields of synthetic microbial ecology and community systems biology have the potential to decrypt these complex relationships. Studying host-associated microbiota across multiple spatial and temporal scales will bridge the gap between individual microorganism studies and large-scale whole community surveys. Here, we discuss the unique potential of Hydra as an emerging experimental model in microbiome research. Through in vivo, in vitro, and in silico approaches the interaction structure of host-associated microbial communities and the effects of the host on the microbiota and its interactions can be disentangled. Research in the model system Hydra can unify disciplines from molecular genetics to ecology, opening up the opportunity to discover fundamental rules that govern microbiome community stability.

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Animal–microbe interactions and the evolution of nervous systems

Cited by 28 publications

References 135 publications

Entomophthovirus: An insect-derived iflavirus that infects a behavior manipulating fungal pathogen of dipterans

Entomophthovirus: An insect-derived iflavirus that infects a behavior manipulating fungal pathogen of dipterans

Introduction to ‘Homology and convergence in nervous system evolution’

Transitioning from Microbiome Composition to Microbial Community Interactions: The Potential of the Metaorganism Hydra as an Experimental Model

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