The Termite Fecal Nest: A Framework for the Opportunistic Acquisition of Beneficial Soil Streptomyces (Actinomycetales: Streptomycetaceae)

Chouvenc, Thomas; Elliott, Monica L.; Šobotník, Jan; Efstathion, Caroline A.; Su, Nan‐Yao

doi:10.1093/ee/nvy152

Cited by 26 publications

(41 citation statements)

References 57 publications

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“…Nest structures are typically constructed from fecal material, which can inhibit the growth of harmful microbes 79 . Termite nests have also been found to harbor beneficial Actinobacteria, which are known to possess antimicrobial activity 35,38 . Colonies can maintain hygienic conditions by cannibalizing nestmates that are infected or have recently succumbed to disease 25,[80][81][82] .…”

Section: Discussionmentioning

confidence: 99%

Increased genetic diversity from colony merging in termites does not improve survival against a fungal pathogen

Aguero

Eyer

Vargo

2020

Sci Rep

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in some species of social insects the increased genetic diversity from having multiple breeders in a colony has been shown to improve pathogen resistance. termite species typically found colonies from single mated pairs and therefore may lack the flexibility to buffer pathogen pressure with increased genetic diversity by varying the initial number of reproductives. However, they can later increase group diversity through colony merging, resulting in a genetically diverse, yet cohesive, workforce. in this study, we investigate whether the increased group diversity from colony fusion benefits social immunity in the subterranean termite Reticulitermes flavipes. We confirm previous findings that colonies of R. flavipes will readily merge and we show that workers will equally groom nestmates and non-nestmates after merging. Despite this, the survival of these merged colonies was not improved after exposure to a fungal pathogen, but instead leveled to that of the more susceptible or the more resistant colony. our study brings little support to the hypothesis that colony fusion may improve immunity through an increase of genetic diversity in R. flavipes. Instead, we find that following exposure to a lethal pathogen, one colony is heavily influential to the entire group's survival after merging. Social insects are among the most abundant and ecologically successful species 1. Their success is inextricably linked to their division of labor where workers engage in different tasks to benefit one or a few reproductives at the expense of their own reproduction. The low number of reproductives in colonies of most species results in high relatedness among nestmate workers, elevating indirect fitness benefits 2. Paradoxically, their social life also entails severe costs, as high worker densities, high relatedness, and closed nests strongly increase the chance of pathogen transmission, which would suggest that these species are vulnerable to disease outbreaks 3. Owing to such pathogenic pressure, social insects have evolved social immunity, whereby individual immune functions and behaviors collectively provide colony-wide disease protection 4-6. Social immunity includes self/allogrooming 7-14 , nest hygiene 15-22 , removal of diseased individuals 23-26 and the use of antimicrobial compounds either produced by individuals or from materials incorporated into the nest 27-38. These diverse immune strategies have undoubtedly reduced the costs of social living, facilitating the success of social insects. Colony resistance to pathogens is also associated with within-colony genetic diversity, as genetically distinct individuals may vary in their susceptibility to different disease strains 39-45. Therefore, a mix of distinct genotypes within a colony interferes with genotype x genotype interactions, such that a pathogen able to infect one genotype may fail to transmit to new hosts if it encounters host genotypes that it cannot infect. Consequently, a genetically diverse colony may reduce the overall spread of a pathogen. Although variatio...

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Section: Discussionmentioning

confidence: 99%

Increased genetic diversity from colony merging in termites does not improve survival against a fungal pathogen

Aguero

Eyer

Vargo

2020

Sci Rep

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“…1D; Heine et al ., 2018) and in the heads of other ants (Liu et al ., 2018). Actinobacteria are also present in the bodies of stingless bees (Rodríguez‐Hernández et al ., 2019), wasps (Madden et al ., 2013) and termites (Sujada, Sungthong & Lumyong, 2014; Chouvenc et al ., 2018; Krishanti et al ., 2018), which produce antimicrobial secretions. Microbial natural products represent an important source for the discovery of potential new antibiotics, with actinomycetes being one of the most prolific groups that produce bioactive compounds (Genilloud, 2018; Niu, 2018).…”

Section: Social Insect Traits and Their Relevance To Ecosystem Servicmentioning

confidence: 99%

The ecosystem services provided by social insects: traits, management tools and knowledge gaps

et al. 2020

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Social insects, i.e. ants, bees, wasps and termites, are key components of ecological communities, and are important ecosystem services (ESs) providers. Here, we review the literature in order to (i) analyse the particular traits of social insects that make them good suppliers of ESs; (ii) compile and assess management strategies that improve the services provided by social insects; and (iii) detect gaps in our knowledge about the services that social insects provide. Social insects provide at least 10 ESs; however, many of them are poorly understood or valued. Relevant traits of social insects include high biomass and numerical abundance, a diversity of mutualistic associations, the ability to build important biogenic structures, versatile production of chemical defences, the simultaneous delivery of several ESs, the presence of castes and division of labour, efficient communication and cooperation, the capacity to store food, and a long lifespan. All these characteristics enhance social insects as ES providers, highlighting their potential, constancy and efficiency as suppliers of these services. In turn, many of these traits make social insects stress tolerant and easy to manage, so increasing the ESs they provide. We emphasise the need for a conservation approach to the management of the services, as well as the potential use of social insects to help restore habitats degraded by human activities. In addition, we stress the need to evaluate both services and disservices in an integrated way, because some species of social insects are among the most problematic invasive species and native pests. Finally, we propose two areas of research that will lead to a greater and more efficient use of social insects as ES providers, and to a greater appreciation of them by producers and decision‐makers.

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“…Hussain et al [3] identified 439 immune-related sequences (i.e., pattern recognition receptors, signal modulators, signal transducers, and effectors) from Coptotermes formosanus Shiraki that were infected by entomopathogenic fungi and bacteria. Some termites and their symbiotic actinobacteria can produce various β-1,3-glucanases and antibiotics to prevent the germination of entomopathogenic fungi [4][5][6]. In addition, termites rely on altered behaviors to protect themselves from microbial pathogens.…”

Section: Introductionmentioning

confidence: 99%

The Effects of Trichoderma Fungi on the Tunneling, Aggregation, and Colony-Initiation Preferences of Black-Winged Subterranean Termites, Odontotermes formosanus (Blattodea: Termitidae)

Xiong

Cai

Chen

et al. 2019

Forests

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The black-winged subterranean termite, Odontotermes formosanus Shiraki, is a severe pest of plantations and forests in China. This termite cultures symbiotic Termitomyces in the fungal combs, which are challenged by antagonistic microbes such as Trichoderma fungi. In a previous study we showed that O. formosanus workers made significantly fewer tunnels in sand containing commercially formulated conidia of Trichoderma viride Pers. ex Fries compared with untreated sand. Herein, we hypothesize that fungi in the genus Trichoderma exert repellent effects on O. formosanus. Different choice tests were conducted to evaluate the tunneling and aggregation behaviors of O. formosanus workers reacting to sand/soil containing the unformulated conidia of seven Trichoderma fungi (Trichoderma longibrachiatum Rifai, Trichoderma koningii Oud., Trichoderma harzianum Rifai, Trichoderma hamatum (Bon.) Bain, Trichoderma atroviride Karsten, Trichoderma spirale Indira and Kamala, and T. viride). We also investigated the colony-initiation preference of paired O. formosanus adults to soil treated with Trichoderma conidia (T. koningii or T. longibrachiatum) versus untreated soil. Tunneling-choice tests showed that sand containing conidia of nearly all Trichoderma fungi tested (except T. harzianum) significantly decreased tunneling activity in O. formosanus workers compared with untreated sand. Aggregation-choice test showed that T. koningii, T. atroviride and T. spirale repelled O. formosanus workers, whereas T. longibrachiatum and T. hamatum attracted termites. There was no significant difference in proportions of paired adults that stayed and laid eggs in the soil blocks treated with conidia of Trichoderma fungi and untreated ones. Our study showed that Trichoderma fungi generally repelled tunneling in O. formosanus, but may exert varied effects on aggregation preference by workers.

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The Termite Fecal Nest: A Framework for the Opportunistic Acquisition of Beneficial Soil Streptomyces (Actinomycetales: Streptomycetaceae)

Cited by 26 publications

References 57 publications

Increased genetic diversity from colony merging in termites does not improve survival against a fungal pathogen

Increased genetic diversity from colony merging in termites does not improve survival against a fungal pathogen

The ecosystem services provided by social insects: traits, management tools and knowledge gaps

The Effects of Trichoderma Fungi on the Tunneling, Aggregation, and Colony-Initiation Preferences of Black-Winged Subterranean Termites, Odontotermes formosanus (Blattodea: Termitidae)

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