Genetic innovations in animal–microbe symbioses

Perreau, Julie; Moran, Nancy A.

doi:10.1038/s41576-021-00395-z

Cited by 92 publications

(87 citation statements)

References 186 publications

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“…The resulting marketplaces of biosynthetic goods and services are recognized as sources of evolutionary innovation (Archibald, 2014). Experimental work on endosymbioses has revealed mechanisms by which the sharing of genes and gene products – once thought to be the sole property of the genomes in which they evolved – gives rise to novel outcomes (Perreau & Moran, 2021). Most of the breakthroughs have however been the result of work, not on lichens, but on other biological systems unearthed after Schwendener’s landmark discovery.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary biology of lichen symbioses

et al. 2022

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Lichens are the symbiotic outcomes of open, interspecies relationships, central to which are a fungus and a phototroph, typically an alga and/or cyanobacterium. The evolutionary processes that led to the global success of lichens are poorly understood. In this review, we explore the goods and services exchange between fungus and phototroph and how this propelled the success of both symbiont and symbiosis. Lichen fungal symbionts count among the only filamentous fungi that expose most of their mycelium to an aerial environment. Phototrophs export carbohydrates to the fungus, which converts them to specific polyols. Experimental evidence suggests that polyols are not only growth and respiratory substrates but also play a role in anhydrobiosis, the capacity to survive desiccation. We propose that this dual functionality is pivotal to the evolution of fungal symbionts, enabling persistence in environments otherwise hostile to fungi while simultaneously imposing costs on growth. Phototrophs, in turn, benefit from fungal protection from herbivory and light stress, while appearing to exert leverage over fungal sex and morphogenesis. Combined with the recently recognized habit of symbionts to occur in multiple symbioses, this creates the conditions for a multiplayer marketplace of rewards and penalties that could drive symbiont selection and lichen diversification.

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Section: Introductionmentioning

confidence: 99%

Evolutionary biology of lichen symbioses

et al. 2022

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“…, microbiomes, makes the elucidation of these mechanisms a formidable challenge. For decades, researchers have turned to nature for other examples of animal-microbe symbioses, which have become powerful models for revealing the basic principles underlying symbiosis [ 4 , 5 ]. Consequently, efforts to document and improve the husbandry techniques associated with these animal hosts will accelerate discovery in the field of symbiosis, which in turn, will help inform strategies to target bacterial symbionts to improve animal and human health.…”

Section: Introductionmentioning

confidence: 99%

Impact of transit time on the reproductive capacity of Euprymna scolopes as a laboratory animal

Cecere

Miyashiro

2022

Lab Anim Res

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Background The Hawaiian bobtail squid Euprymna scolopes hosts various marine bacterial symbionts, and these symbioses have served as models for the animal-microbe relationships that are important for host health. Within a light organ, E. scolopes harbors populations of the bacterium Vibrio fischeri, which produce low levels of bioluminescence that the squid uses for camouflage. The symbiosis is initially established after a juvenile squid hatches from its egg and acquires bacterial symbionts from the ambient marine environment. The relative ease with which a cohort of wild-caught E. scolopes can be maintained in a mariculture facility has facilitated over 3 decades of research involving juvenile squid. However, because E. scolopes is native to the Hawaiian archipelago, their transport from Hawaii to research facilities often represents a stress that has the potential to impact their physiology. Results Here, we describe animal survival and reproductive capacity associated with a cohort of squid assembled from two shipments with markedly different transit times. We found that the lower juvenile squid counts generated by animals with the longer transit time were not due to the discrepancy in shipment but instead to fewer female squid that produced egg clutches at an elevated rate, which we term hyper-reproductivity. We find that hyper-reproductive females were responsible for 58% of the egg clutches laid. Conclusions The significance of these findings for E. scolopes biology and husbandry is discussed, thereby providing a platform for future investigation and further development of this cephalopod as a valuable lab animal for microbiology research.

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“…Symbioses are traditionally distinguished by being open (symbionts are environmentally acquired, resulting in frequent HGT and average or high GC content), closed (symbionts are parentally transmitted, resulting in the absence of HGT, low GC content, and genome degradation), or mixed (symbionts are mainly parentally transmitted, but occasional environmental acquisition occurs) ( Perreau and Moran 2022 ). Here, we observe that the Bathymodiolus symbionts are environmentally transmitted, do not engage frequently in HGT, and have an average GC content of 38%.…”

Section: Discussionmentioning

confidence: 99%

Pangenome Evolution in Environmentally Transmitted Symbionts of Deep-Sea Mussels Is Governed by Vertical Inheritance

Picazo

Werner

Kupczok

2022

Genome Biology and Evolution

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Microbial pangenomes vary across species; their size and structure are determined by genetic diversity within the population and by gene loss and horizontal gene transfer (HGT). Many bacteria are associated with eukaryotic hosts where the host colonization dynamics may impact bacterial genome evolution. Host-associated lifestyle has been recognized as a barrier to HGT in parentally transmitted bacteria. However, pangenome evolution of environmentally acquired symbionts remains understudied, often due to limitations in symbiont cultivation. Using high-resolution metagenomics, here we study pangenome evolution of two co-occurring endosymbionts inhabiting Bathymodiolus brooksi mussels from a single cold seep. The symbionts, sulfur-oxidizing (SOX) and methane-oxidizing (MOX) gamma-proteobacteria, are environmentally acquired at an early developmental stage and individual mussels may harbor multiple strains of each symbiont species. We found differences in the accessory gene content of both symbionts across individual mussels, which are reflected by differences in symbiont strain composition. Compared to core genes, accessory genes are enriched in genome plasticity functions. We found no evidence for recent horizontal gene transfer between both symbionts. A comparison between the symbiont pangenomes revealed that the MOX population is less diverged and contains fewer accessory genes, supporting that the MOX association with B. brooksi is more recent in comparison to that of SOX. Our results show that the pangenomes of both symbionts evolved mainly by vertical inheritance. We conclude that genome evolution of environmentally transmitted symbionts that associate with individual hosts over their lifetime is affected by a narrow symbiosis where the frequency of HGT is constrained.

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Genetic innovations in animal–microbe symbioses

Cited by 92 publications

References 186 publications

Evolutionary biology of lichen symbioses

Evolutionary biology of lichen symbioses

Impact of transit time on the reproductive capacity of Euprymna scolopes as a laboratory animal

Pangenome Evolution in Environmentally Transmitted Symbionts of Deep-Sea Mussels Is Governed by Vertical Inheritance

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