Compartmentalization drives the evolution of symbiotic cooperation

Chomicki, Guillaume; Werner, Gijsbert D. A.; West, Stuart A.; Kiers, E. Toby

doi:10.1098/rstb.2019.0602

Cited by 73 publications

(77 citation statements)

References 156 publications

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“…T. endolucinida both had the additional potential to utilize methanol as a source of energy and carbon with an xox-type methanol dehydrogenase and the serine pathway for C1-carbon incorporation into biomass. Compartmentalizing coexisting symbiont species into separate bacteriocytes could prevent direct competition by allowing the host to partition resources and discriminate cooperative symbionts from potential cheaters that might destabilize the symbiosis (45). Consistent with this, our FISH analyses showed that although symbiont species cooccurred in host individuals they never cooccurred in single host bacteriocytes (Fig.…”

Section: Discussionsupporting

confidence: 79%

Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

Osvatic

Wilkins

Leibrecht

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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In the ocean, most hosts acquire their symbionts from the environment. Due to the immense spatial scales involved, our understanding of the biogeography of hosts and symbionts in marine systems is patchy, although this knowledge is essential for understanding fundamental aspects of symbiosis such as host–symbiont specificity and evolution. Lucinidae is the most species-rich and widely distributed family of marine bivalves hosting autotrophic bacterial endosymbionts. Previous molecular surveys identified location-specific symbiont types that “promiscuously” form associations with multiple divergent cooccurring host species. This flexibility of host–microbe pairings is thought to underpin their global success, as it allows hosts to form associations with locally adapted symbionts. We used metagenomics to investigate the biodiversity, functional variability, and genetic exchange among the endosymbionts of 12 lucinid host species from across the globe. We report a cosmopolitan symbiont species, Candidatus Thiodiazotropha taylori, associated with multiple lucinid host species. Ca. T. taylori has achieved more success at dispersal and establishing symbioses with lucinids than any other symbiont described thus far. This discovery challenges our understanding of symbiont dispersal and location-specific colonization and suggests both symbiont and host flexibility underpin the ecological and evolutionary success of the lucinid symbiosis.

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Section: Discussionsupporting

confidence: 79%

Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

Osvatic

Wilkins

Leibrecht

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…The selection of a particular species or population in a segment of a gradient immediately influences the gradient itself (for instance consuming O 2 , or lowering the pH), or create new associated gradients, as gradients of nutrients, inhibitory substances, quorum-sensing molecules, or pheromones, contributing to the fluidity of the multidimensional niche landscape, and the intensity of biotic interactions. That facilitate genetic exchanges with neighboring kin populations sharing the same selective compartment, increasing the evolvability of the lineage ( Chomicki et al, 2020 ).…”

Section: Niches Gradients and Bacterial Diversificationmentioning

confidence: 99%

The Origin of Niches and Species in the Bacterial World

et al. 2021

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Niches are spaces for the biological units of selection, from cells to complex communities. In a broad sense, “species” are biological units of individuation. Niches do not exist without individual organisms, and every organism has a niche. We use “niche” in the Hutchinsonian sense as an abstraction of a multidimensional environmental space characterized by a variety of conditions, both biotic and abiotic, whose quantitative ranges determine the positive or negative growth rates of the microbial individual, typically a species, but also parts of the communities of species contained in this space. Microbial organisms (“species”) constantly diversify, and such diversification (radiation) depends on the possibility of opening up unexploited or insufficiently exploited niches. Niche exploitation frequently implies “niche construction,” as the colonized niche evolves with time, giving rise to new potential subniches, thereby influencing the selection of a series of new variants in the progeny. The evolution of niches and organisms is the result of reciprocal interacting processes that form a single unified process. Centrifugal microbial diversification expands the limits of the species’ niches while a centripetal or cohesive process occurs simultaneously, mediated by horizontal gene transfers and recombinatorial events, condensing all of the information recovered during the diversifying specialization into “novel organisms” (possible future species), thereby creating a more complex niche, where the selfishness of the new organism(s) establishes a “homeostatic power” limiting the niche’s variation. Once the niche’s full carrying capacity has been reached, reproductive isolation occurs, as no foreign organisms can outcompete the established population/community, thereby facilitating speciation. In the case of individualization-speciation of the microbiota, its contribution to the animal’ gut structure is a type of “niche construction,” the result of crosstalk between the niche (host) and microorganism(s). Lastly, there is a parallelism between the hierarchy of niches and that of microbial individuals. The increasing anthropogenic effects on the biosphere (such as globalization) might reduce the diversity of niches and bacterial individuals, with the potential emergence of highly transmissible multispecialists (which are eventually deleterious) resulting from the homogenization of the microbiosphere, a possibility that should be explored and prevented.

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“…Prior studies on isolated RNA sequences have pointed toward the possibility that encapsulation and related biophysical effects could increase ribozyme and aptamer activity ( 34 , 35 , 68 ), but the generality of these findings has been unclear. In addition, while compartmentalization is known to be important for the evolution of cooperative phenotypes ( 69 – 71 ), the evolutionary consequences of RNA encapsulation on noncooperative phenotypes have been largely unstudied, despite being the subject of speculations ( 13 , 72 – 74 ). Here, we present a systematic study of the effect of encapsulation for five different ribozyme families, previously derived from an exhaustive search of sequence space for self-aminoacylating RNAs, representing three distinct ribozyme motifs and including tens of thousands of different mutant sequences.…”

Section: Discussionmentioning

confidence: 99%

Encapsulation of ribozymes inside model protocells leads to faster evolutionary adaptation

Lai

Liu

Chen

2021

Proc. Natl. Acad. Sci. U.S.A.

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Functional biomolecules, such as RNA, encapsulated inside a protocellular membrane are believed to have comprised a very early, critical stage in the evolution of life, since membrane vesicles allow selective permeability and create a unit of selection enabling cooperative phenotypes. The biophysical environment inside a protocell would differ fundamentally from bulk solution due to the microscopic confinement. However, the effect of the encapsulated environment on ribozyme evolution has not been previously studied experimentally. Here, we examine the effect of encapsulation inside model protocells on the self-aminoacylation activity of tens of thousands of RNA sequences using a high-throughput sequencing assay. We find that encapsulation of these ribozymes generally increases their activity, giving encapsulated sequences an advantage over nonencapsulated sequences in an amphiphile-rich environment. In addition, highly active ribozymes benefit disproportionately more from encapsulation. The asymmetry in fitness gain broadens the distribution of fitness in the system. Consistent with Fisher’s fundamental theorem of natural selection, encapsulation therefore leads to faster adaptation when the RNAs are encapsulated inside a protocell during in vitro selection. Thus, protocells would not only provide a compartmentalization function but also promote activity and evolutionary adaptation during the origin of life.

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Compartmentalization drives the evolution of symbiotic cooperation

Cited by 73 publications

References 156 publications

Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

The Origin of Niches and Species in the Bacterial World

Encapsulation of ribozymes inside model protocells leads to faster evolutionary adaptation

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