Animal host–microbe interactions

Hoye, Bethany J.; Fenton, Andy

doi:10.1111/1365-2656.12788

Cited by 15 publications

(9 citation statements)

References 47 publications

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“…Our results further emphasize the importance of using novel model organisms to study host-microbe interactions and highlight the importance of the microbiome for health and fitness of a host in general. We further assume that bacterial diversity and species abundances within the microbiome are balanced on the polyp, most likely due to interbacterial (11,40,41,83) and host-microbe interactions (31,86) as well as host genotype (87,88). However, the molecular mechanism of the microbial contribution to A. aurita fitness, in particular, to asexual reproduction, has to be elucidated in the future.…”

Section: Discussionmentioning

confidence: 99%

The Native Microbiome is Crucial for Offspring Generation and Fitness of Aurelia aurita

Weiland‐Bräuer

Pinnow

Langfeldt

et al. 2020

mBio

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All multicellular organisms are associated with microbial communities, ultimately forming a metaorganism. Several studies conducted on well-established model organisms point to immunological, metabolic, and behavioral benefits of the associated microbiota for the host. Consequently, a microbiome can influence the physiology of a host; moreover, microbial community shifts can affect host health and fitness. The present study aimed to evaluate the significance and functional role of the native microbiota for life cycle transitions and fitness of the cnidarian moon jellyfish Aurelia aurita. A comprehensive host fitness experiment was conducted studying the polyp life stage and integrating 12 combinations of treatments with microbiota modification (sterile conditions, foreign food bacteria, and potential pathogens). Asexual reproduction, e.g., generation of daughter polyps, and the formation and release of ephyrae were highly affected in the absence of the native microbiota, ultimately resulting in a halt of strobilation and ephyra release. Assessment of further fitness traits showed that health, growth, and feeding rate were decreased in the absence and upon community changes of the native microbiota, e.g., when challenged with selected bacteria. Moreover, changes in microbial community patterns were detected by 16S rRNA amplicon sequencing during the course of the experiment. This demonstrated that six operational taxonomic units (OTUs) significantly correlated and explained up to 97% of fitness data variability, strongly supporting the association of impaired fitness with the absence/presence of specific bacteria. Conclusively, our study provides new insights into the importance and function of the microbiome for asexual reproduction, health, and fitness of the basal metazoan A. aurita. IMPORTANCE All multicellular organisms are associated with a diverse and specific community of microorganisms; consequently, the microbiome is of fundamental importance for health and fitness of the multicellular host. However, studies on microbiome contribution to host fitness are in their infancy, in particular, for less well-established hosts such as the moon jellyfish Aurelia aurita. Here, we studied the impact of the native microbiome on the asexual reproduction and on further fitness traits (health, growth, and feeding) of the basal metazoan due to induced changes in its microbiome. We observed significant impact on all fitness traits analyzed, in particular, in the absence of the protective microbial shield and when challenged with marine potentially pathogenic bacterial isolates. Notable is the identified crucial importance of the native microbiome for the generation of offspring, consequently affecting life cycle decisions. Thus, we conclude that the microbiome is essential for the maintenance of a healthy metaorganism.

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Section: Discussionmentioning

confidence: 99%

The Native Microbiome is Crucial for Offspring Generation and Fitness of Aurelia aurita

Weiland‐Bräuer

Pinnow

Langfeldt

et al. 2020

mBio

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“…Gut microbiota influences multiple features of the host’s biology, including nutrient acquisition, immune response, metabolism, behavior, and life-history traits (Broderick and Lemaitre, 2012; Douglas, 2018a; Hoye and Fenton, 2018). In general, gut microbiota influences phenotypic variation exhibited by host organisms, which can contribute speeding up the adaptive response under changing and fluctuating environments (Alberdi et al, 2016; Macke et al, 2017; Romano, 2017).…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota ofDrosophila subobscuracontributes to its heat tolerance but is sensitive to transient thermal stress

Jaramillo

Castañeda

2021

Preprint

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Global warming impacts the animal’s fitness, leading to increasing extinction risk in ectotherm species. Gut microbiota can contribute to host physiology leading to an increase of resistance to abiotic stress conditions. Temperature has profound effects on ectotherms and gut microbiota can influence cold and heat tolerance of ectotherm species. Additionally, the gut microbiota is sensitive to environmental temperature, which induces changes in its composition and diversity. Here, we investigated the role of the gut microbiota on heat tolerance of Drosophila subobscura, comparing the knockdown time between conventional and axenic, and we also assessed the impact of heat stress on the diversity and community structure of the gut microbiota, comparing non-stressed and heat-stressed flies. Our findings provide evidence that gut microbiota influences heat tolerance, and that heat stress modifies the gut microbiota at taxonomical and structural levels. These results demonstrate that gut microbiota contributes to heat tolerance but it is also highly sensitive to transient heat stress, which could have important effects on host fitness, population risk extinction, and vulnerability of ectotherms to current and future climatic conditions.

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“…These systems provide resources and benefits not found in other species and have bolstered research on the microbiome, enabling key discoveries about mechanistic, ecological and evolutionary interactions with microorganisms [ 2 , 3 ]. While these traditional systems remain essential to this research, new systems are being developed to address specific questions and expand the diversity of experimental systems (e.g., Apis –microbiome, Cockroaches–microbiome, Heteropteran– Burkholderia , Hydra –bacteria systems) [ 4 , 5 , 6 , 7 , 8 ]. New organisms in animal–microbe research are emphasizing work on (1) pathogenic organisms, (2) mutualistic intracellular symbionts, and (3) the extracellular communities of microorganisms present on epithelia surfaces—known as the microbiome.…”

Section: Modern Systems Of Symbiosis Researchmentioning

confidence: 99%

Rediscovering a Forgotten System of Symbiosis: Historical Perspective and Future Potential

Martinson

2020

Genes

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While the majority of symbiosis research is focused on bacteria, microbial eukaryotes play important roles in the microbiota and as pathogens, especially the incredibly diverse Fungi kingdom. The recent emergence of widespread pathogens in wildlife (bats, amphibians, snakes) and multidrug-resistant opportunists in human populations (Candida auris) has highlighted the importance of better understanding animal–fungus interactions. Regardless of their prominence there are few animal–fungus symbiosis models, but modern technological advances are allowing researchers to utilize novel organisms and systems. Here, I review a forgotten system of animal–fungus interactions: the beetle–fungus symbioses of Drugstore and Cigarette beetles with their symbiont Symbiotaphrina. As pioneering systems for the study of mutualistic symbioses, they were heavily researched between 1920 and 1970, but have received only sporadic attention in the past 40 years. Several features make them unique research organisms, including (1) the symbiont is both extracellular and intracellular during the life cycle of the host, and (2) both beetle and fungus can be cultured in isolation. Specifically, fungal symbionts intracellularly infect cells in the larval and adult beetle gut, while accessory glands in adult females harbor extracellular fungi. In this way, research on the microbiota, pathogenesis/infection, and mutualism can be performed. Furthermore, these beetles are economically important stored-product pests found worldwide. In addition to providing a historical perspective of the research undertaken and an overview of beetle biology and their symbiosis with Symbiotaphrina, I performed two analyses on publicly available genomic data. First, in a preliminary comparative genomic analysis of the fungal symbionts, I found striking differences in the pathways for the biosynthesis of two B vitamins important for the host beetle, thiamine and biotin. Second, I estimated the most recent common ancestor for Drugstore and Cigarette beetles at 8.8–13.5 Mya using sequence divergence (CO1 gene). Together, these analyses demonstrate that modern methods and data (genomics, transcriptomes, etc.) have great potential to transform these beetle–fungus systems into model systems again.

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Animal host–microbe interactions

Cited by 15 publications

References 47 publications

The Native Microbiome is Crucial for Offspring Generation and Fitness of Aurelia aurita

The Native Microbiome is Crucial for Offspring Generation and Fitness of Aurelia aurita

Gut microbiota ofDrosophila subobscuracontributes to its heat tolerance but is sensitive to transient thermal stress

Rediscovering a Forgotten System of Symbiosis: Historical Perspective and Future Potential

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