The female organs of symbiont transmission in the Eumolpinae

ABSTRACTFor insects that depend on one or more bacterial endosymbionts for survival, it is critical that these bacteria are faithfully transmitted between insect generations. Cicadas harbor two essential bacterial endosymbionts, “CandidatusSulcia muelleri” and “CandidatusHodgkinia cicadicola.” In some cicada species,Hodgkiniahas fragmented into multiple distinct but interdependent cellular and genomic lineages that can differ in abundance by more than two orders of magnitude. This complexity presents a potential problem for the host cicada, because low-abundance but essentialHodgkinialineages risk being lost during the symbiont transmission bottleneck from mother to egg. Here we show that all cicada eggs seem to receive the full complement ofHodgkinialineages, and that in cicadas with more complexHodgkiniathis outcome is achieved by increasing the number ofHodgkiniacells transmitted by up to 6-fold. We further show that cicada species with varyingHodgkiniacomplexity do not visibly alter their transmission mechanism at the resolution of cell biological structures. Together these data suggest that a major cicada adaptation to changes in endosymbiont complexity is an increase in the number ofHodgkiniacells transmitted to each egg. We hypothesize that the requirement to increase the symbiont titer is one of the costs associated withHodgkiniafragmentation.IMPORTANCESap-feeding insects critically rely on one or more bacteria or fungi to provide essential nutrients that are not available at sufficient levels in their diets. These microbes are passed between insect generations when the mother places a small packet of microbes into each of her eggs before it is laid. We have previously described an unusual lineage fragmentation process in a nutritional endosymbiotic bacterium of cicadas calledHodgkinia. In some cicadas, a singleHodgkinialineage has split into numerous related lineages, each performing a subset of original function and therefore each required for normal host function. Here we test how this splitting process affects symbiont transmission to eggs. We find that cicadas dramatically increase the titer ofHodgkiniacells passed to each egg in response to lineage fragmentation, and we hypothesize that this increase in bacterial cell count is one of the major costs associated with endosymbiont fragmentation.

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Enhancement of antimicrobial diversity in situ through relaxed symbiont specificity in an insect/actinomycete partnership

10.1101/2020.12.02.394189 ◽

2020 ◽

Author(s):

Rita de Cassia Pessotti ◽

Bridget L. Hansen ◽

Jewel N. Reaso ◽

Javier A. Ceja-Navarro ◽

Laila El-Hifnawi ◽

...

Keyword(s):

Social Behavior ◽

Metarhizium Anisopliae ◽

Phylogenetic Analyses ◽

Pathogen Resistance ◽

Transmission Mechanism ◽

Fecal Material ◽

Fungal Entomopathogen ◽

Symbiont Transmission ◽

Chemical Strategies

ABSTRACTSome insects form symbioses in which actinomycetes provide defense against pathogens by making antimicrobials. The range of chemical strategies employed across these symbioses, and how these strategies relate to insect social behavior and mechanisms of symbiont transmission, remains underexplored. Here, we assess subsocial passalid beetles Odontotaenius disjunctus (known as bessbugs), and their frass (fecal material), as a model insect/actinomycete system. Through chemical and phylogenetic analyses, we found that O. disjunctus associates with an exceptionally wide variety of actinomycetes and antimicrobials. Metabolites detected directly in frass displayed both synergistic and antagonistic inhibition of a fungal entomopathogen, Metarhizium anisopliae, and multiple streptomycete isolates inhibited this pathogen when co-cultivated directly in frass. Together, these findings support a model in which coprophagy as a vertical transmission mechanism leads to relaxed symbiote specificity, resulting in a rich and dynamic repertoire of antimicrobials that insulates O. disjunctus against the evolution of pathogen resistance.

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Simulated folivory increases vertical transmission of fungal endophytes that deter herbivores and alter tolerance to herbivory in Poa autumnalis

Annals of Botany ◽

10.1093/aob/mcaa021 ◽

2020 ◽

Vol 125 (6) ◽

pp. 981-991 ◽

Cited By ~ 2

Author(s):

Pedro E Gundel ◽

Prudence Sun ◽

Nikki D Charlton ◽

Carolyn A Young ◽

Tom E X Miller ◽

...

Keyword(s):

Vertical Transmission ◽

Transmission Rate ◽

Horizontal Transmission ◽

Fungal Endophytes ◽

Natural Populations ◽

Plant Tolerance ◽

Hyphal Density ◽

Symbiotic Fungi ◽

Symbiont Transmission ◽

Fitness Benefits

Abstract Background and Aims The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission? Methods We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission. Key Results Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission. Conclusions Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.

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Observation of asexual reproduction with symbiont transmission in planktonic foraminifera

Journal of Plankton Research ◽

10.1093/plankt/fbaa033 ◽

2020 ◽

Vol 42 (4) ◽

pp. 403-410 ◽

Cited By ~ 3

Author(s):

Haruka Takagi ◽

Atsushi Kurasawa ◽

Katsunori Kimoto

Keyword(s):

Life Cycle ◽

Sexual Reproduction ◽

Vertical Transmission ◽

Asexual Reproduction ◽

Planktonic Foraminifera ◽

Gamete Release ◽

Symbiotic Algae ◽

Laboratory Cultures ◽

Symbiont Transmission

Abstract Gamete release has been frequently observed in laboratory cultures of various species of planktonic foraminifera. Those observations have been taken as evidence that these organisms produce new generations exclusively by sexual reproduction. We report here the first observation of asexual reproduction in Globigerinita uvula, a small, microperforate foraminifera. The asexual phase was associated with the release of ca. 110 offspring, all of which hosted symbiotic algae that must have been passed on directly from the parent. This event was also the first observation of vertical transmission of symbionts in planktonic foraminifera. Although the trigger of the observed asexual reproduction and its frequency in nature remain unknown, our observation indicates that among the planktonic foraminifera, at least G. uvula has not abandoned the asexual phase of its life cycle.

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Mothers never miss the moment: a fine-tuned mechanism for vertical symbiont transmission in a subsocial insect

Animal Behaviour ◽

10.1016/j.anbehav.2011.11.006 ◽

2012 ◽

Vol 83 (1) ◽

pp. 293-300 ◽

Cited By ~ 35

Author(s):

Takahiro Hosokawa ◽

Mantaro Hironaka ◽

Hiromi Mukai ◽

Koichi Inadomi ◽

Nobuhiko Suzuki ◽

...

Keyword(s):

Symbiont Transmission ◽

The Moment

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Interaction between Workers during a Short Time Window Is Required for Bacterial Symbiont Transmission in Acromyrmex Leaf-Cutting Ants

PLoS ONE ◽

10.1371/journal.pone.0103269 ◽

2014 ◽

Vol 9 (7) ◽

pp. e103269 ◽

Cited By ~ 21

Author(s):

Sarah E. Marsh ◽

Michael Poulsen ◽

Adrián Pinto-Tomás ◽

Cameron R. Currie

Keyword(s):

Time Window ◽

Bacterial Symbiont ◽

Short Time Window ◽

Symbiont Transmission ◽

Leaf Cutting ◽

Short Time

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

10.1101/412882 ◽

2018 ◽

Cited By ~ 2

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.

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

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2020.600318 ◽

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.

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Host’s guardian protein counters degenerative symbiont evolution

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2103957118 ◽

2021 ◽

Vol 118 (25) ◽

pp. e2103957118

Author(s):

Ryuichi Koga ◽

Masahiko Tanahashi ◽

Naruo Nikoh ◽

Takahiro Hosokawa ◽

Xian-Ying Meng ◽

...

Keyword(s):

Vertical Transmission ◽

Host Protein ◽

Capsule Production ◽

Symbiont Transmission ◽

Essential Function ◽

Nymphal Growth ◽

Female Specific ◽

Odorant Binding ◽

Harsh Conditions ◽

Insight Into

Microbial symbioses significantly contribute to diverse organisms, where long-lasting associations tend to result in symbiont genome erosion, uncultivability, extinction, and replacement. How such inherently deteriorating symbiosis can be harnessed to stable partnership is of general evolutionary interest. Here, we report the discovery of a host protein essential for sustaining symbiosis. Plataspid stinkbugs obligatorily host an uncultivable and genome-reduced gut symbiont, Ishikawaella. Upon oviposition, females deposit “capsules” for symbiont delivery to offspring. Within the capsules, the fragile symbiotic bacteria survive the harsh conditions outside the host until acquired by newborn nymphs to establish vertical transmission. We identified a single protein dominating the capsule content, which is massively secreted by female-specific intestinal organs, embedding the symbiont cells, and packaged into the capsules. Knockdown of the protein resulted in symbiont degeneration, arrested capsule production, symbiont transmission failure, and retarded nymphal growth, unveiling its essential function for ensuring symbiont survival and vertical transmission. The protein originated from a lineage of odorant-binding protein-like multigene family, shedding light on the origin of evolutionary novelty regarding symbiosis. Experimental suppression of capsule production extended the female’s lifespan, uncovering a substantial cost for maintaining symbiosis. In addition to the host’s guardian protein, the symbiont’s molecular chaperone, GroEL, was overproduced in the capsules, highlighting that the symbiont’s eroding functionality is compensated for by stabilizer molecules of host and symbiont origins. Our finding provides insight into how intimate host–symbiont associations can be maintained over evolutionary time despite the symbiont’s potential vulnerability to degeneration and malfunctioning.

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Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata

10.1101/264796 ◽

2018 ◽

Author(s):

Kate M. Quigley ◽

Bette L. Willis ◽

Carly D. Kenkel

Keyword(s):

Thermal Tolerance ◽

Coral Species ◽

Early Life History ◽

Amplicon Sequencing ◽

Life History Stages ◽

Genetic Mechanisms ◽

Symbiont Transmission ◽

Plastic Changes ◽

Cell Densities ◽

Symbiont Shuffling

AbstractAdult organisms may “prime” their offspring for environmental change through a number of genetic and non-genetic mechanisms, termed parental effects. Some coral species can alter their thermal tolerance by shuffling the proportions of Symbiodinium types within their endosymbiotic communities, but it is unclear if this plasticity can be transferred to offspring in corals that have maternal symbiont transmission. We evaluated symbiont community composition in tagged colonies of Montipora digitata from Orpheus Island, Australia, over two successive annual spawning seasons, the second of which overlapped with the 2016 mass coral bleaching event on the Great Barrier Reef. We applied amplicon sequencing of the ITS2 locus to samples of four families (parent colonies and 10-12 eggs per family) to characterize their potential for symbiont shuffling and to determine if shuffled abundances were preserved in gametes. Symbiont cell densities and photochemical efficiencies of the symbionts’ photosystem II differed significantly among adults in 2016, suggesting differential responses to increased temperatures. Although abundances of the dominant symbiont haplotype, a representative of clade C15, did not differ among families or over time, low-abundance (“background”) ITS2 types differed more among years (2015 vs. 2016) than between life stages (parent vs. offspring). Results indicate that background symbiont shuffling can occur in a canonically ‘stable’ symbiosis, and that such plastic changes to the symbiont community are heritable. To our knowledge, this is the first evidence that shuffled Symbiodinium communities can be inherited by early life-history stages and supports the hypothesis that plastic changes in microbial communities may serve as a mechanism of rapid coral acclimation to changing environmental conditions.

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