scholarly journals Insect-Microbe Mutualism without Vertical Transmission: a Stinkbug Acquires a Beneficial Gut Symbiont from the Environment Every Generation

2007 ◽  
Vol 73 (13) ◽  
pp. 4308-4316 ◽  
Author(s):  
Yoshitomo Kikuchi ◽  
Takahiro Hosokawa ◽  
Takema Fukatsu
Keyword(s):  
Vertical Transmission ◽  
Bacterial Symbiont ◽  
Transmission Mode ◽  
Dense Population ◽  
Insect Midgut ◽  
Riptortus Clavatus ◽  
Host Insect ◽  
Host Fitness ◽  
Fitness Effects ◽  
Posterior Midgut

ABSTRACT The broad-headed bug Riptortus clavatus (Heteroptera: Alydidae) possesses a number of crypts at a posterior midgut region, which house a dense population of a bacterial symbiont belonging to the genus Burkholderia. Although the symbiont is highly prevalent (95 to 100%) in the host populations, the symbiont phylogeny did not reflect the host systematics at all. In order to understand the mechanisms underlying the promiscuous host-symbiont relationship despite the specific and prevalent association, we investigated the transmission mode and the fitness effects of the Burkholderia symbiont in R. clavatus. Inspection of eggs and a series of rearing experiments revealed that the symbiont is not vertically transmitted but is environmentally acquired by nymphal insects. The Burkholderia symbiont was present in the soil of the insect habitat, and a culture strain of the symbiont was successfully isolated from the insect midgut. Rearing experiments by using sterilized soybean bottles demonstrated that the cultured symbiont is able to establish a normal and efficient infection in the host insect, and the symbiont infection significantly improves the host fitness. These results indicated that R. clavatus postnatally acquires symbiont of a beneficial nature from the environment every generation, uncovering a previously unknown pathway through which a highly specific insect-microbe association is maintained. We suggest that the stinkbug-Burkholderia relationship may be regarded as an insect analogue of the well-known symbioses between plants and soil-associated microbes, such as legume-Rhizobium and alder-Frankia relationships, and we discuss the evolutionary relevance of the mutualistic but promiscuous insect-microbe association.

scholarly journals Evolution of symbiont transmission in conditional mutualisms in spatially and temporally variable environments

2020 ◽  
Author(s):  
Alexandra Brown ◽  
Erol Akçay
Keyword(s):  
Vertical Transmission ◽  
Horizontal Transmission ◽  
Environmental Variation ◽  
Transmission Mode ◽  
Trade Off ◽  
Symbiotic Relationships ◽  
Physiological Constraints ◽  
Fitness Effects ◽  
Variable Environments ◽  
Symbiont Transmission

AbstractSymbiotic relationships affect the fitness and organismal function of virtually all organisms. In many cases, the fitness effects of symbiosis may be beneficial or harmful depending on the environment. The hosts of such symbionts are favored to acquire them only when the symbiont is beneficial. However, it is not clear whether such selection favors vertical or horizontal transmission, both, or neither. To address this question, we model the evolution of transmission mode in a conditional mutualism experiencing spatial and temporal environmental variation. We find that when symbionts affect host lifespan, but not fecundity, horizontal transmission can contain them to beneficial environments. Vertical transmission can produce symbiont containment when the environmental state is synchronized across locations. We also find an emergent trade-off between horizontal and vertical transmission, suggesting that physiological constraints are not required for the evolution of limits on the total amount of transmission.

Development of common leaf-footed bug pests depends on the presence and identity of their environmentally-acquired symbionts

2022 ◽  
Author(s):  
Martha S. Hunter ◽  
Edwin F. Umanzor ◽  
Suzanne E. Kelly ◽  
Shaira Marie Whitaker ◽  
Alison Ravenscraft
Keyword(s):  
Life History ◽  
Pest Management ◽  
Vertical Transmission ◽  
Growth And Development ◽  
Performance Outcomes ◽  
Bacterial Symbiont ◽  
Future Studies ◽  
Fitness Effects ◽  
Obligate Symbiont

Many beneficial symbioses between bacteria and their terrestrial arthropod hosts are vertically transmitted from mother to offspring, ensuring the progeny acquire necessary partners. Unusually, in several families of coreoid and lygeoid bugs (Hemiptera), nymphs must instead ingest the beneficial symbiont, Burkholderia ( sensu lato ), from the environment early in development. We studied the effects of Burkholderia on development of two species of leaf-footed bug (Coreidae) in the genus Leptoglossus, L. zonatus and L. phyllopus. We found no evidence for vertical transmission of the symbiont, but found stark differences in performance between symbiotic and aposymbiotic individuals. Symbiotic nymphs grew more rapidly, were approximately four times more likely to survive to adulthood than aposymbiotic bugs, and were two times larger. These findings suggest that Burkholderia is an obligate symbiont for Leptoglossus species. We also tested for variation in fitness effects conferred by four symbiont isolates representing different species within Burkholderia ’s insect-associated Stinkbug Beneficial and Environmental (SBE) clade. While three isolates conferred similar benefits to hosts, nymphs associated with the fourth isolate grew more slowly and weighed significantly less as adults. The effects of the four isolates were similar for both Leptoglossus species. This work indicates that both Burkholderia acquisition and isolate identity play critical roles in the growth and development of Leptoglossus. Importance Leptoglossus zonatus and L. phyllopus are important polyphagous pests and both species have been well-studied, but generally without regard to their dependance on a bacterial symbiont. Our results indicate that the central role of Burkholderia in the biology of these insects, as well as in other leaf-footed bugs, should be considered in future studies of coreid life history, ecology and pest management. Our work suggests acquisition of Burkholderia is critical for the growth and development of Leptoglossus species. Further, we found that there was variation in performance outcomes according to symbiont identity, even among members of the Stinkbug Beneficial and Environmental clade. This suggests that although environmental acquisition of a symbiont can provide extraordinary flexibility in partner associations, it also carries a risk if the partner is sub-optimal.

scholarly journals Genome Analysis of “Candidatus Regiella insecticola” Strain TUt, Facultative Bacterial Symbiont of the Pea Aphid Acyrthosiphon pisum

2020 ◽  
Vol 9 (40) ◽  
Author(s):  
Naruo Nikoh ◽  
Tsutomu Tsuchida ◽  
Ryuichi Koga ◽  
Kenshiro Oshima ◽  
Masahira Hattori ◽  
...  
Keyword(s):  
Genome Analysis ◽  
Acyrthosiphon Pisum ◽  
Draft Genome ◽  
Bacterial Symbiont ◽  
Pea Aphid ◽  
Adaptive Traits ◽  
Host Insect

ABSTRACT The genome of “Candidatus Regiella insecticola” strain TUt, a facultative bacterial symbiont of the pea aphid Acyrthosiphon pisum, was analyzed. We determined a 2.5-Mb draft genome consisting of 14 contigs; this will contribute to the understanding of the symbiont, which underpins various ecologically adaptive traits of the host insect.

scholarly journals A de novo approach to inferring within-host fitness effects during untreated HIV-1 infection

2020 ◽  
Vol 16 (6) ◽  
pp. e1008171
Author(s):  
Christopher J. R. Illingworth ◽  
Jayna Raghwani ◽  
David Serwadda ◽  
Nelson K. Sewankambo ◽  
Merlin L. Robb ◽  
...  
Keyword(s):  
De Novo ◽  
Host Fitness ◽  
Fitness Effects ◽  
Hiv 1

scholarly journals Capsule-Transmitted Gut Symbiotic Bacterium of the Japanese Common Plataspid Stinkbug, Megacopta punctatissima

2002 ◽  
Vol 68 (1) ◽  
pp. 389-396 ◽  
Author(s):  
Takema Fukatsu ◽  
Takahiro Hosokawa
Keyword(s):  
Bacterial Species ◽  
Symbiotic Bacterium ◽  
Egg Mass ◽  
Polymorphism Analysis ◽  
Host Insect ◽  
Fitness Effects ◽  
Body Coloration ◽  
Molecular Phylogenetic ◽  
Microbiological Aspects

ABSTRACT The Japanese common plataspid stinkbug, Megacopta punctatissima, deposits small brown particles, or symbiont capsules, on the underside of the egg mass for the purpose of transmission of symbiotic bacteria to the offspring. We investigated the microbiological aspects of the bacteria contained in the capsule, such as microbial diversity, phylogenetic placement, localization in vivo, and fitness effects on the host insect. Restriction fragment length polymorphism analysis of 16S ribosomal DNA clones revealed that a single bacterial species dominates the microbiota in the capsule. The bacterium was not detected in the eggs but in the capsules, which unequivocally demonstrated that the bacterium is transmitted to the offspring of the insect orally rather than transovarially, through probing of the capsule content. Molecular phylogenetic analysis showed that the bacterium belongs to the γ-subdivision of the Proteobacteria. In adult insects the bacterium was localized in the posterior section of the midgut. Deprivation of the bacterium from the nymphs resulted in retarded development, arrested growth, abnormal body coloration, and other symptoms, suggesting that the bacterium is essential for normal development and growth of the host insect.

scholarly journals Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses

2018 ◽  
Author(s):  
Shelbi L Russell
Keyword(s):  
Vertical Transmission ◽  
Horizontal Transmission ◽  
Transmission Mode ◽  
Symbiotic Associations ◽  
Transmission Modes ◽  
Symbiont Transmission ◽  
Environment Type ◽  
Full Separation ◽  
Host Evolution ◽  
Host Tissues

AbstractSymbiotic associations between bacteria and eukaryotes exhibit a range of transmission strategies. Anecdotal observations suggest that symbionts of terrestrial hosts tend to be strictly vertically inherited through host tissues, whereas symbionts of marine hosts tend towards horizontal transmission. Aside from a few cursory investigations, the rates and distributions of transmission modes have not been investigated in depth across associations, despite the consequences for symbiont and host evolution. To address this empirically and estimate the rate of each mode, I compiled data from the literature and for associations between transmission mode and the environment, transmission route, symbiont function, and taxa involved in the symbiosis. Of the 441 analyzed symbioses, 50.1% were strictly vertically transmitted, 34.0% exhibited some form of mixed mode transmission, and 15.9% were strictly horizontally transmitted. Binning symbioses by their environment revealed a significant skew towards vertical transmission on land and horizontal transmission in aquatic environments, with mixed modes abundant in both. However, host and symbiont taxa were not randomly distributed, which prevented the full separation of these variables. Overall, the data suggest that many symbiotic taxa are capable of horizontal transmission and barriers exist that reduce the rate of these events. Thus, both the environment type and host/symbiont taxa combined influence symbiont transmission mode evolution.One sentence summaryThrough an intensive analysis of the literature on symbiosis transmission modes, estimated rates for each transmission mode were calculated, revealing bias for horizontal transmission in the ocean and vertical transmission on land.

scholarly journals Can Differences in Symbiont Transmission Mode Explain the Abundance and Distribution of Fungus-Growing Termites in West Africa?

2020 ◽  
Vol 8 ◽  
Author(s):  
Judith Korb ◽  
Simon Kolotchèlèma Silué ◽  
N'golo Abdoulaye Koné
Keyword(s):  
Vertical Transmission ◽  
National Parks ◽  
Horizontal Transmission ◽  
Species Abundance ◽  
Transmission Mode ◽  
Termite Species ◽  
Symbiont Transmission ◽  
Ecological Dominance ◽  
Study Sites ◽  
Abundance And Distribution

Fungus-growing termites (Isoptera: Macrotermitinae) dominate African savannah ecosystems where they play important roles in ecosystem functioning. Their ecological dominance in these ecosystems has been attributed to living in an ectosymbiosis with fungi of the genus Termitomyces (Lyophyllaceae). Evolutionary theory predicts that the transmission mode of a symbiont determines cooperation and conflict between host and symbiont with vertical transmission (co-transmission of host and symbiont offspring to the next generation) leading to less conflict than horizontal transmission (symbionts are acquired by the host from the environment). Thus, one can hypothesize associations with vertical transmission to be ecological more successful than those with horizontal transmission. We tested this by analyzing whether there is an association between transmission mode and fungus-growing termite species abundance and distribution in West-African savannah and forest ecosystems. We used data from a total of 78 study sites comprising protected National Parks as well as anthropogenically disturbed ecosystems, covering Benin, Côte d'Ivoire, and Togo. Our results showed that, in contrast to expectation, species with horizontal symbiont transmission were more common. We encountered more often species with horizontal than vertical transmission. This result might be due to the fact that only five out of the 25 identified fungus-growing termite species had vertical transmission. Yet, species with horizontal transmission also had higher relative abundances within study sites than those with vertical transmission. Thus, transmission mode is unlikely to explain abundance differences between fungus-growing termite species.

scholarly journals Disentangling the Relative Roles of Vertical Transmission, Subsequent Colonizations, and Diet on Cockroach Microbiome Assembly

mSphere ◽  
2021 ◽  
Vol 6 (1) ◽  
Author(s):  
Justinn Renelies-Hamilton ◽  
Kristjan Germer ◽  
David Sillam-Dussès ◽  
Kasun H. Bodawatta ◽  
Michael Poulsen
Keyword(s):  
Gut Microbiota ◽  
Microbial Communities ◽  
Vertical Transmission ◽  
Priority Effects ◽  
Rrna Gene ◽  
Combined Effects ◽  
Microbial Composition ◽  
Host Fitness ◽  
Microbial Invasion ◽  
Host Taxon

ABSTRACT A multitude of factors affect the assemblies of complex microbial communities associated with animal hosts, with implications for community flexibility, resilience, and long-term stability; however, their relative effects have rarely been deduced. Here, we use a tractable lab model to quantify the relative and combined effects of parental transmission (egg case microbiome present/reduced), gut inocula (cockroach versus termite gut provisioned), and varying diets (matched or unmatched with gut inoculum source) on gut microbiota structure of hatchlings of the omnivorous cockroach Shelfordella lateralis using 16S rRNA gene (rDNA) amplicon sequencing. We show that the presence of a preexisting bacterial community via vertical transmission of microbes on egg cases reduces subsequent microbial invasion, suggesting priority effects that allow initial colonizers to take a strong hold and which stabilize the microbiome. However, subsequent inoculation sources more strongly affect ultimate community composition and their ecological networks, with distinct host-taxon-of-origin effects on which bacteria establish. While this is so, communities respond flexibly to specific diets in ways that consequently impact predicted community functions. In conclusion, our findings suggest that inoculations drive communities toward different stable states depending on colonization and extinction events, through ecological host-microbe relations and interactions with other gut bacteria, while diet in parallel shapes the functional capabilities of these microbiomes. These effects may lead to consistent microbial communities that maximize the extended phenotype that the microbiota provides the host, particularly if microbes spend most of their lives in host-associated environments. IMPORTANCE When host fitness is dependent on gut microbiota, microbial community flexibility and reproducibility enhance host fitness by allowing fine-tuned environmental tracking and sufficient stability for host traits to evolve. Our findings lend support to the importance of vertically transmitted early-life microbiota as stabilizers, through interactions with potential colonizers, which may contribute to ensuring that the microbiota aligns within host fitness-enhancing parameters. Subsequent colonizations are driven by microbial composition of the sources available, and we confirm that host-taxon-of-origin affects stable subsequent communities, while communities at the same time retain sufficient flexibility to shift in response to available diets. Microbiome structure is thus the result of the relative impact and combined effects of inocula and fluctuations driven by environment-specific microbial sources and digestive needs. These affect short-term community structure on an ecological time scale but could ultimately shape host species specificities in microbiomes across evolutionary time, if environmental conditions prevail.

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