Host and symbiont jointly control gut microbiota during complete metamorphosis

Johnston, Paul R.

doi:10.1603/ice.2016.94147

Cited by 35 publications

(54 citation statements)

References 27 publications

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“…However, the majority of the larval gut microbiota are purged during metamorphosis (Kingsley , Hammer et al. ; but see Johnston and Rolff ). It is more likely that these members of the gut flora are common in both butterflies and other insects because they are generally adapted to the insect gut environment (e.g., Chouaia et al.…”

Section: Discussionmentioning

confidence: 99%

Structure and function of the bacterial and fungal gut microbiota of Neotropical butterflies

Ravenscraft

Berry

Hammer

et al. 2019

Ecological Monographs

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The relationship between animals and their gut flora is simultaneously one of the most common and most complex symbioses on Earth. Despite its ubiquity, our understanding of this invisible but often critical relationship is still in its infancy. We employed adult Neotropical butterflies as a study system to ask three questions: First, how does gut microbial community composition vary across host individuals, species and dietary guilds? Second, how do gut microbiota compare to food microbial communities? Finally, are gut flora functionally adapted to the chemical makeup of host foods? To answer these questions we captured nearly 300 Costa Rican butterflies representing over 50 species, six families, and two feeding guilds: frugivores and nectivores. We characterized bacteria and fungi in guts, wild fruits, and wild nectars via amplicon sequencing and assessed the catabolic abilities of the gut microbiota via culture‐based assays. Gut communities were distinct from food communities, suggesting that the gut environment acts as a filter on potential colonists. Nevertheless, gut flora varied widely among individuals and species. On average, a pair of butterflies shared 21% of their bacterial species and 6% of their fungi. Host species explained 25–30% of variation in microbial communities while host diet explained 4%, suggesting that non‐dietary aspects of host biology play a large role in structuring the butterfly gut flora. Much of the variation between species correlated with host phylogeny. Host diet was related to gut microbial function: compared to frugivores, nectivores’ gut flora exhibited increased catabolism of sugars and sugar alcohols and decreased catabolism of amino acids, carboxylic acids, and dicarboxylic acids. Since fermented juice contains more amino acids and less sugar than nectar, it appears that host diet filters the gut flora by favoring microbes that digest compounds abundant in foods. By quantifying the degree to which gut communities vary among host individuals, species and dietary guilds and evaluating how gut microbial composition and catabolic potential are related to host diet, this study highlights the linkages between structure and function in one of the most complex and ubiquitous symbioses in the animal kingdom.

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Section: Discussionmentioning

confidence: 99%

Structure and function of the bacterial and fungal gut microbiota of Neotropical butterflies

Ravenscraft

Berry

Hammer

et al. 2019

Ecological Monographs

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“…It is known that the microbiome is of high importance in maintaining homeostasis of the host's body (Russell & Dunn, ; Chatelier et al., ). A recent study showed that host and symbiont communities cooperatively interact to maintain the midgut microbiota in a symbiotic balance (Johnston & Rolff, ), suggesting that the host needs more control over symbionts by means of AMP proteins. Symbionts may become pathogenic if they grow and reproduce uncontrollably, diverting resources away from growth and other needs of the host if not controlled by the host's immune system (Erdogan & Rao, ; Fujimori, ).…”

Section: Discussionmentioning

confidence: 99%

“…Streptococcus faecalis Andrewes and Horder) in the midgut of G. mellonella (Jarosz, ; Johnston & Rolff, ). This microbe is a heritable nutrient‐providing symbiont of G. mellonella (Bucher, ; Johnston & Rolff, ) that is transmitted vertically, from mother to offspring (Chen et al., ). It is probably among those rare microorganisms that can survive under the antibacterial properties of the G. mellonella diet.…”

Section: Discussionmentioning

confidence: 99%

Food quality affects the expression of antimicrobial peptide genes upon simulated parasite attack in the larvae of greater wax moth

Krams

Kecko

Inashkina

et al. 2017

Entomologia Exp Applicata

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Predator‐prey interactions are an important evolutionary force affecting the immunity of the prey. Parasitoids and mites pierce the cuticle of their prey, which respond by activating their immune system against predatory attacks. Immunity is a costly function for the organism, as it often competes with other life‐history traits for limited nutrients. We tested whether the expression of antimicrobial peptides (AMP) of the larvae of the greater wax moth Galleria mellonella (L.) (Lepidoptera: Pyralidae) changes as a consequence of insertion of a nylon monofilament, which acts like a synthetic parasite. The treatment was done for larvae grown on a high‐quality vs. a low‐quality diet. The expression of Gloverin and 6‐tox were upregulated in response to the insertion of the nylon monofilament. The expression of 6‐tox, Cecropin‐D, and Gallerimycin were significantly higher in the ‘low‐quality diet’ group than in the ‘high‐quality diet’ group. As food quality seems to affect AMP gene expression in G. mellonella larvae, it should always be controlled for in studies on bacterial and fungal infections in G. mellonella.

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“…Holometabolous insects, such as the Hymenoptera, shed the entire inner larval gut epithelium including their gut content during metamorphosis (Hakim, Baldwin, & Smagghe, ), which can lead to the clearance of symbionts from the gut. However, in some holometabolous insects, gut symbionts persist through metamorphosis due to actions of the host, the symbiont, or both (e.g., Johnston & Rolff, ). This might explain why in some attine ants late stage pupae do not differ from older workers in either absolute abundance of bacteria or in gut community diversity (Zhukova et al, ).…”

Section: Introductionmentioning

confidence: 99%

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

Segers

Kaltenpoth

Foitzik

2019

Ecology and Evolution

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Gut bacteria aid their host in digestion and pathogen defense, and bacterial communities that differ in diversity or composition may vary in their ability to do so. Typically, the gut microbiomes of animals living in social groups converge as members share a nest environment and frequently interact. Social insect colonies, however, consist of individuals that differ in age, physiology, and behavior, traits that could affect gut communities or that expose the host to different bacteria, potentially leading to variation in the gut microbiome within colonies. Here we asked whether bacterial communities in the abdomen of Temnothorax nylanderi ants, composed largely of the gut microbiome, differ between different reproductive and behavioral castes. We compared microbiomes of queens, newly eclosed workers, brood carers, and foragers by high‐throughput 16S rRNA sequencing. Additionally, we sampled individuals from the same colonies twice, in the field and after 2 months of laboratory housing. To disentangle the effects of laboratory environment and season on microbial communities, additional colonies were collected at the same location after 2 months. There were no large differences between ant castes, although queens harbored more diverse microbial communities than workers. Instead, we found effects of colony, environment, and season on the abdominal microbiome. Interestingly, colonies with more diverse communities had produced more brood. Moreover, the queens' microbiome composition was linked to egg production. Although long‐term coevolution between social insects and gut bacteria has been repeatedly evidenced, our study is the first to find associations between abdominal microbiome characteristics and colony productivity in social insects.

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Host and symbiont jointly control gut microbiota during complete metamorphosis

Cited by 35 publications

References 27 publications

Structure and function of the bacterial and fungal gut microbiota of Neotropical butterflies

Structure and function of the bacterial and fungal gut microbiota of Neotropical butterflies

Food quality affects the expression of antimicrobial peptide genes upon simulated parasite attack in the larvae of greater wax moth

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

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