Microbiota in Insects

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Systems Microbiology".

Deadline for manuscript submissions: closed (31 March 2022) | Viewed by 37841

Special Issue Editor

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, UMR Ecologie Microbienne, F-69622 Villeurbanne, France
Interests: fungal ecology; fungal diversity (metataxogenomic and functional diversity); mosquito-microbiota interactions; mycobiota; Asian tiger mosquito

Special Issue Information

Dear Colleagues,

Studies focusing on insect-associated microbiota have highlighted that microorganisms influence many aspects of host biology, such as development, survival, reproduction, immunity, behavior or even vector competence. This means that insects can no longer be considered as isolated entities and instead should be considered as inseparable from their microbiota with which they interact and form a holobiont. However, the understanding of insect–microbiota relationships as well as molecular mechanisms underlying symbiotic interactions is still scarce and has been mainly limited either to bacteria or to phytophagous insects. Insect-associated microbiota is composed of complex microbial communities (bacteria, fungi, protists, viruses, and nematodes) with various biological functions that deserve further exploration. Better knowledge of the role of microbiota in insect biology is thus essential to maintain insect diversity conservation or promote the development of new pest and vector control strategies.

Concerning this Special Issue of the journal Microorganisms, we cordially invite you to submit research papers, review articles or short communications presenting recent advances related to our knowledge of insect–microbiota interactions in terms of microbiota functions, molecular mechanisms of interactions, environmental impacts on insect–microbiota, insect–microbiota coevolution, and microbiota-based strategies for pest or vector control.

Dr. Patricia Luis
Guest Editor

Manuscript Submission Information

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Keywords

  • Insect holobiont 
  • Microbiota functions 
  • Microbiota diversity and environmental impacts
  • Complex multipartite interactions 
  • Molecular mechanisms of symbiotic interactions 
  • Insect–microbiota coevolution 
  • Pest or vector control

Published Papers (11 papers)

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Research

Jump to: Review

18 pages, 3006 KiB  
Article
Assessing the Tsetse Fly Microbiome Composition and the Potential Association of Some Bacteria Taxa with Trypanosome Establishment
by Calmes Ursain Bouaka Tsakeng, Tito Tresor Melachio Tanekou, Steve Feudjio Soffack, Inaki Tirados, Cedrique Noutchih, Flobert Njiokou, Jude Daiga Bigoga and Charles Sinclair Wondji
Microorganisms 2022, 10(6), 1141; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10061141 - 31 May 2022
Cited by 3 | Viewed by 2000
Abstract
The tsetse flies, biological vectors of African trypanosomes, harbour a variety of bacteria involved in their vector competence that may help in developing novel vector control tools. This study provides an inventory of tsetse bacterial communities in Cameroon and explores their possible associations [...] Read more.
The tsetse flies, biological vectors of African trypanosomes, harbour a variety of bacteria involved in their vector competence that may help in developing novel vector control tools. This study provides an inventory of tsetse bacterial communities in Cameroon and explores their possible associations with trypanosome establishment in Glossina palpalis palpalis. High throughput sequencing of the V3-V4 hypervariable region of the bacterial 16S rRNA gene, with subsequent metagenomic, multivariate, and association analyses, were used to investigate the levels and patterns of microbial diversity in four tsetse species. Overall, 31 bacterial genera and four phyla were identified. The primary symbiont Wigglesworthia dominated almost all the samples, with an overall relative abundance of 47.29%, and seemed to be replaced by Serratia or Burkholderia in some G. tachinoides flies. Globally, significant differences were observed in the microbiome diversity and composition among tsetse species and between teneral and non-teneral flies, or between flies displaying or not displaying mature trypanosome infections. In addition, differential abundance testing showed some OTUs, or some bacteria taxa, associated with trypanosome maturation in tsetse flies. These bacteria could be further investigated for an understanding of their mechanism of action and alternatively, transformed and used to block trypanosome development in tsetse flies. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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12 pages, 1297 KiB  
Article
Endosymbiotic Bacterial Diversity of Corn Leaf Aphid, Rhopalosiphum maidis Fitch (Hemiptera: Aphididae) Associated with Maize Management Systems
by Artúr Botond Csorba, Ciprian George Fora, János Bálint, Tamás Felföldi, Attila Szabó, István Máthé, Hugh D. Loxdale, Endre Kentelky, Imre-István Nyárádi and Adalbert Balog
Microorganisms 2022, 10(5), 939; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10050939 - 30 Apr 2022
Cited by 6 | Viewed by 3501
Abstract
In this study, different maize fields cultivated under different management systems were sampled to test corn leaf aphid, Rhopalosiphum maidis, populations in terms of total and endosymbiotic bacterial diversity. Corn leaf aphid natural populations were collected from traditionally managed maize fields grown [...] Read more.
In this study, different maize fields cultivated under different management systems were sampled to test corn leaf aphid, Rhopalosiphum maidis, populations in terms of total and endosymbiotic bacterial diversity. Corn leaf aphid natural populations were collected from traditionally managed maize fields grown under high agricultural and natural landscape diversity as well as conventionally treated high-input agricultural fields grown in monoculture and with fertilizers use, hence with low natural landscape diversity. Total bacterial community assessment by DNA sequencing was performed using the Illumina MiSeq platform. In total, 365 bacterial genera were identified and 6 endosymbiont taxa. A high abundance of the primary endosymbiont Buchnera and secondary symbionts Serratia and Wolbachia were detected in all maize crops. Their frequency was found to be correlated with the maize management system used, probably with fertilizer input. Three other facultative endosymbionts (“Candidatus Hamiltonella”, an uncultured Rickettsiales genus, and Spiroplasma) were also recorded at different frequencies under the two management regimes. Principal components analyses revealed that the relative contribution of the obligate and dominant symbiont Buchnera to the aphid endosymbiotic bacterial community was 72%, whereas for the managed system this was only 16.3%. When facultative symbionts alone were considered, the effect of management system revealed a DNA diversity of 23.3%. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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14 pages, 3272 KiB  
Article
Dynamics of the Queensland Fruit Fly Microbiome through the Transition from Nature to an Established Laboratory Colony
by Rajib Majumder, Phillip W. Taylor and Toni A. Chapman
Microorganisms 2022, 10(2), 291; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10020291 - 26 Jan 2022
Cited by 5 | Viewed by 2401
Abstract
The transition from nature to laboratory or mass rearing can impose significant physiological and evolutionary impact on insects. The Queensland fruit fly (also known as ‘Qfly’), Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), is a serious economic pest that presents major challenges for horticulture industries [...] Read more.
The transition from nature to laboratory or mass rearing can impose significant physiological and evolutionary impact on insects. The Queensland fruit fly (also known as ‘Qfly’), Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), is a serious economic pest that presents major challenges for horticulture industries in Australia. The sterile insect technique (SIT) is being developed to manage outbreaks in regions that remain free of Qfly and to suppress populations in regions where this species is endemic. The biology of Qfly is intimately connected to its microbiome. Therefore, changes in the microbiome that occur through domestication have implications for SIT. There are numerous studies of the microbiome in Qfly larvae and adults, but there is little information on how the microbiome changes as Qfly laboratory colonies are established. In this study, high-throughput Illumina sequencing was used to assess the Qfly microbiome in colonies reared from wild larvae, collected from fruit, for five generations, on a gel-based larval diet. Beta diversity analysis showed that the bacterial communities from Generation 5 (G5) clustered separately from earlier generations. At the genus level, bacterial communities were significantly different between the generations and mostly altered at G5. However, communities were found similar at phyla to family taxonomic levels. We observed high abundance of Morganella and Burkholderia at the genus level in the larval and pupal stages respectively at G5, but these were not detected in earlier generations. Overall, our findings demonstrate that the domestication process strongly affects the Qfly microbiome and prompts questions about the functional relationship between the Qfly and its microbiome, as well as implications for the performance of insects that have been domesticated and mass-reared for SIT programs. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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15 pages, 3809 KiB  
Article
Antifungal Streptomyces spp., Plausible Partners for Brood-Caring of the Dung Beetle Copris tripartitus
by Sung Hun Kim, Goeun Park, Jin-Soo Park and Hak Cheol Kwon
Microorganisms 2021, 9(9), 1980; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9091980 - 17 Sep 2021
Cited by 5 | Viewed by 2168
Abstract
The dung beetle Copris tripartitus Waterhouse (Coleoptera: Scarabaeidae) is a coprophagous insect that lives in and feeds primarily on the feces of mammalian herbivores and is known to protect their offspring from the pathogen-rich environment by performing parental care for brood balls. Brood [...] Read more.
The dung beetle Copris tripartitus Waterhouse (Coleoptera: Scarabaeidae) is a coprophagous insect that lives in and feeds primarily on the feces of mammalian herbivores and is known to protect their offspring from the pathogen-rich environment by performing parental care for brood balls. Brood balls under continuous management by dung beetle are rarely contaminated by entomopathogenic fungi compared to abandoned brood balls. On the supposition that dung beetles may benefit from mutualistic bacteria that protect their offspring against fungal pathogens, we evaluated the antifungal activities of bacteria isolated from the dung beetle and brood ball. As a result, bacterial isolates, mainly streptomycetes, manifested potent and broad-spectrum antifungal activity against various fungi, including entomopathogens. Of the isolates, Streptomyces sp. AT67 exhibited pronounced antifungal activities. Culture-dependent and independent approaches show that this strain has occurred continuously in dung beetles that were collected over three years. Moreover, metabolic profiling and chemical investigation demonstrated that the strain produced an antifungal polyene macrocyclic lactam, sceliphrolactam, as a major product. Our findings imply that specific symbiotic bacteria of C. tripartitus are likely to contribute brood ball hygiene by inhibiting fungal parasites in the environment. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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22 pages, 2260 KiB  
Article
Culture-Independent and Culture-Dependent Characterization of the Black Soldier Fly Gut Microbiome Reveals a Large Proportion of Culturable Bacteria with Potential for Industrial Applications
by Dorothee Tegtmeier, Sabine Hurka, Sanja Mihajlovic, Maren Bodenschatz, Stephanie Schlimbach and Andreas Vilcinskas
Microorganisms 2021, 9(8), 1642; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9081642 - 31 Jul 2021
Cited by 22 | Viewed by 4131
Abstract
Black soldier fly larvae (BSFL) are fast-growing, resilient insects that can break down a variety of organic substrates and convert them into valuable proteins and lipids for applications in the feed industry. Decomposition is mediated by an abundant and versatile gut microbiome, which [...] Read more.
Black soldier fly larvae (BSFL) are fast-growing, resilient insects that can break down a variety of organic substrates and convert them into valuable proteins and lipids for applications in the feed industry. Decomposition is mediated by an abundant and versatile gut microbiome, which has been studied for more than a decade. However, little is known about the phylogeny, properties and functions of bacterial isolates from the BSFL gut. We therefore characterized the BSFL gut microbiome in detail, evaluating bacterial diversity by culture-dependent methods and amplicon sequencing of the 16S rRNA gene. Redundant strains were identified by genomic fingerprinting and 105 non-redundant isolates were then tested for their ability to inhibit pathogens. We cultivated representatives of 26 genera, covering 47% of the families and 33% of the genera detected by amplicon sequencing. Among these isolates, we found several representatives of the most abundant genera: Morganella, Enterococcus, Proteus and Providencia. We also isolated diverse members of the less-abundant phylum Actinobacteria, and a novel genus of the order Clostridiales. We found that 15 of the isolates inhibited at least one of the tested pathogens, suggesting a role in helping to prevent colonization by pathogens in the gut. The resulting culture collection of unique BSFL gut bacteria provides a promising resource for multiple industrial applications. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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15 pages, 1525 KiB  
Article
Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host
by Morgane Ourry, Agathe Crosland, Valérie Lopez, Stéphane A. P. Derocles, Christophe Mougel, Anne-Marie Cortesero and Denis Poinsot
Microorganisms 2021, 9(6), 1313; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9061313 - 16 Jun 2021
Cited by 8 | Viewed by 2758
Abstract
Facultative intracellular symbionts like the α-proteobacteria Wolbachia influence their insect host phenotype but little is known about how much they affect their host microbiota. Here, we quantified the impact of Wolbachia infection on the bacterial community of the cabbage root fly Delia radicum [...] Read more.
Facultative intracellular symbionts like the α-proteobacteria Wolbachia influence their insect host phenotype but little is known about how much they affect their host microbiota. Here, we quantified the impact of Wolbachia infection on the bacterial community of the cabbage root fly Delia radicum by comparing the microbiota of Wolbachia-free and infected adult flies of both sexes. We used high-throughput DNA sequencing (Illumina MiSeq, 16S rRNA, V5-V7 region) and performed a community and a network analysis. In both sexes, Wolbachia infection significantly decreased the diversity of D. radicum bacterial communities and modified their structure and composition by reducing abundance in some taxa but increasing it in others. Infection by Wolbachia was negatively correlated to 8 bacteria genera (Erwinia was the most impacted), and positively correlated to Providencia and Serratia. We suggest that Wolbachia might antagonize Erwinia for being entomopathogenic (and potentially intracellular), but would favor Providencia and Serratia because they might protect the host against chemical plant defenses. Although they might seem prisoners in a cell, endocellular symbionts can impact the whole microbiota of their host, hence its extended phenotype, which provides them with a way to interact with the outside world. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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15 pages, 2310 KiB  
Article
Bacterial Microbiota of Field-Collected Helicoverpa zea (Lepidoptera: Noctuidae) from Transgenic Bt and Non-Bt Cotton
by Jean M. Deguenon, Anirudh Dhammi, Loganathan Ponnusamy, Nicholas V. Travanty, Grayson Cave, Roger Lawrie, Dan Mott, Dominic Reisig, Ryan Kurtz and R. Michael Roe
Microorganisms 2021, 9(4), 878; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9040878 - 20 Apr 2021
Cited by 10 | Viewed by 2604
Abstract
The bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), is an important agricultural pest in U.S. cotton and is managed using transgenic hybrids that produce insecticidal proteins from the bacterium, Bacillus thuringiensis (Bt). The reduced efficacy against H. zea caterpillars of Bt plants expressing Cry [...] Read more.
The bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), is an important agricultural pest in U.S. cotton and is managed using transgenic hybrids that produce insecticidal proteins from the bacterium, Bacillus thuringiensis (Bt). The reduced efficacy against H. zea caterpillars of Bt plants expressing Cry toxins is increasing in the field. In a first step towards understanding Bt cotton–bollworm–microbiota interactions, we investigated the internal bacterial microbiota of second–third stadium H. zea collected in the field from non-Bt versus Bt (WideStrike) cotton in close proximity (in North Carolina, USA). The bacterial populations were analyzed using culture-dependent and -independent molecular approaches. We found that WideStrike samples had a higher bacterial density and diversity per larva than insects collected from non-Bt cotton over two field seasons: 8.42 ± 0.23 and 5.36 ± 0.75 (log10 colony forming units per insect) for WideStrike compared to 6.82 ± 0.20 and 4.30 ± 0.56 for non-Bt cotton for seasons 1 and 2, respectively. Fifteen phyla, 103 families, and 229 genera were identified after performing Illumina sequencing of the 16S rRNA. At the family level, Enterobacteriaceae and Enterococcaceae were the most abundant taxa. The Enterococcaceae family was comprised mostly of Enterococcus species (E. casseliflavus and another Enterococcus sp.). Members of the Enterococcus genus can acidify their environment and can potentially reduce the alkaline activation of some Bt toxins. These findings argue for more research to better understand the role of cotton–bollworm–bacteria interactions and the impact on Bt toxin caterpillar susceptibility. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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17 pages, 10522 KiB  
Article
New Insights on the Zeugodacus cucurbitae (Coquillett) Bacteriome
by Elias Asimakis, Panagiota Stathopoulou, Apostolis Sapounas, Kanjana Khaeso, Costas Batargias, Mahfuza Khan and George Tsiamis
Microorganisms 2021, 9(3), 659; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9030659 - 22 Mar 2021
Cited by 5 | Viewed by 2651
Abstract
Various factors, including the insect host, diet, and surrounding ecosystem can shape the structure of the bacterial communities of insects. We have employed next generation, high-throughput sequencing of the 16S rRNA to characterize the bacteriome of wild Zeugodacus (Bactrocera) cucurbitae (Coquillett) [...] Read more.
Various factors, including the insect host, diet, and surrounding ecosystem can shape the structure of the bacterial communities of insects. We have employed next generation, high-throughput sequencing of the 16S rRNA to characterize the bacteriome of wild Zeugodacus (Bactrocera) cucurbitae (Coquillett) flies from three regions of Bangladesh. The tested populations developed distinct bacterial communities with differences in bacterial composition, suggesting that geography has an impact on the fly bacteriome. The dominant bacteria belonged to the families Enterobacteriaceae, Dysgomonadaceae and Orbaceae, with the genera Dysgonomonas, Orbus and Citrobacter showing the highest relative abundance across populations. Network analysis indicated variable interactions between operational taxonomic units (OTUs), with cases of mutual exclusion and copresence. Certain bacterial genera with high relative abundance were also characterized by a high degree of interactions. Interestingly, genera with a low relative abundance like Shimwellia, Gilliamella, and Chishuiella were among those that showed abundant interactions, suggesting that they are also important components of the bacterial community. Such knowledge could help us identify ideal wild populations for domestication in the context of the sterile insect technique or similar biotechnological methods. Further characterization of this bacterial diversity with transcriptomic and metabolic approaches, could also reveal their specific role in Z. cucurbitae physiology. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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Review

Jump to: Research

22 pages, 1525 KiB  
Review
Molecular Rationale of Insect-Microbes Symbiosis—From Insect Behaviour to Mechanism
by Sujata Singh, Archana Singh, Varsha Baweja, Amit Roy, Amrita Chakraborty and Indrakant Kumar Singh
Microorganisms 2021, 9(12), 2422; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9122422 - 24 Nov 2021
Cited by 11 | Viewed by 3290
Abstract
Insects nurture a panoply of microbial populations that are often obligatory and exist mutually with their hosts. Symbionts not only impact their host fitness but also shape the trajectory of their phenotype. This co-constructed niche successfully evolved long in the past to mark [...] Read more.
Insects nurture a panoply of microbial populations that are often obligatory and exist mutually with their hosts. Symbionts not only impact their host fitness but also shape the trajectory of their phenotype. This co-constructed niche successfully evolved long in the past to mark advanced ecological specialization. The resident microbes regulate insect nutrition by controlling their host plant specialization and immunity. It enhances the host fitness and performance by detoxifying toxins secreted by the predators and abstains them. The profound effect of a microbial population on insect physiology and behaviour is exploited to understand the host–microbial system in diverse taxa. Emergent research of insect-associated microbes has revealed their potential to modulate insect brain functions and, ultimately, control their behaviours, including social interactions. The revelation of the gut microbiota–brain axis has now unravelled insects as a cost-effective potential model to study neurodegenerative disorders and behavioural dysfunctions in humans. This article reviewed our knowledge about the insect–microbial system, an exquisite network of interactions operating between insects and microbes, its mechanistic insight that holds intricate multi-organismal systems in harmony, and its future perspectives. The demystification of molecular networks governing insect–microbial symbiosis will reveal the perplexing behaviours of insects that could be utilized in managing insect pests. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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17 pages, 679 KiB  
Review
Microorganisms Associated with Mosquito Oviposition Sites: Implications for Habitat Selection and Insect Life Histories
by Maxime Girard, Edwige Martin, Laurent Vallon, Vincent Raquin, Christophe Bellet, Yves Rozier, Emmanuel Desouhant, Anne-Emmanuelle Hay, Patricia Luis, Claire Valiente Moro and Guillaume Minard
Microorganisms 2021, 9(8), 1589; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9081589 - 26 Jul 2021
Cited by 10 | Viewed by 4511
Abstract
Mosquitoes are considered one of the most important threats worldwide due to their ability to vector pathogens. They are responsible for the transmission of major pathogens such as malaria, dengue, zika, or chikungunya. Due to the lack of treatments or prophylaxis against many [...] Read more.
Mosquitoes are considered one of the most important threats worldwide due to their ability to vector pathogens. They are responsible for the transmission of major pathogens such as malaria, dengue, zika, or chikungunya. Due to the lack of treatments or prophylaxis against many of the transmitted pathogens and an increasing prevalence of mosquito resistance to insecticides and drugs available, alternative strategies are now being explored. Some of these involve the use of microorganisms as promising agent to limit the fitness of mosquitoes, attract or repel them, and decrease the replication and transmission of pathogenic agents. In recent years, the importance of microorganisms colonizing the habitat of mosquitoes has particularly been investigated since they appeared to play major roles in their development and diseases transmission. In this issue, we will synthesize researches investigating how microorganisms present within water habitats may influence breeding site selection and oviposition strategies of gravid mosquito females. We will also highlight the impact of such microbes on the fate of females’ progeny during their immature stages with a specific focus on egg hatching, development rate, and larvae or pupae survival. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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20 pages, 1289 KiB  
Review
Diversity and Functions of Yeast Communities Associated with Insects
by Simon Malassigné, Guillaume Minard, Laurent Vallon, Edwige Martin, Claire Valiente Moro and Patricia Luis
Microorganisms 2021, 9(8), 1552; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9081552 - 21 Jul 2021
Cited by 19 | Viewed by 5427
Abstract
Following the concept of the holobiont, insect-microbiota interactions play an important role in insect biology. Many examples of host-associated microorganisms have been reported to drastically influence insect biological processes such as development, physiology, nutrition, survival, immunity, or even vector competence. While a huge [...] Read more.
Following the concept of the holobiont, insect-microbiota interactions play an important role in insect biology. Many examples of host-associated microorganisms have been reported to drastically influence insect biological processes such as development, physiology, nutrition, survival, immunity, or even vector competence. While a huge number of studies on insect-associated microbiota have focused on bacteria, other microbial partners including fungi have been comparatively neglected. Yeasts, which establish mostly commensal or symbiotic relationships with their host, can dominate the mycobiota of certain insects. This review presents key advances and progress in the research field highlighting the diversity of yeast communities associated with insects, as well as their impact on insect life-history traits, immunity, and behavior. Full article
(This article belongs to the Special Issue Microbiota in Insects)
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