Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Symbiotic relationships promote biological diversification by unlocking new ecological niches. Over evolutionary time, hosts and symbionts often enter intimate and permanent relationships, which must be maintained and regulated for both lineages to persist. Many insect species harbor obligate, heritable symbiotic bacteria that provision essential nutrients and enable hosts to exploit niches that would otherwise be unavailable. Hosts must regulate symbiont population sizes, but optimal regulation may be affected by the need to respond to the ongoing evolution of symbionts, which experience high levels of genetic drift and potential selection for selfish traits. We address the extent of intraspecific variation in the regulation of a mutually obligate symbiosis, between the pea aphid (Acyrthosiphon pisum) and its maternally transmitted symbiont, Buchnera aphidicola. Using experimental crosses to identify effects of host genotypes, we measured symbiont titer, as the ratio of genomic copy numbers of symbiont and host, as well as developmental time and fecundity of hosts. We find a large (>10-fold) range in symbiont titer among genetically distinct aphid lines harboring the same Buchnera haplotype. Aphid clones also vary in fitness, measured as developmental time and fecundity, and genetically based variation in titer is correlated with host fitness, with higher titers corresponding to lower reproductive rates of hosts. Our work shows that obligate symbiosis is not static but instead is subject to short-term evolutionary dynamics, potentially reflecting coevolutionary interactions between host and symbiont.

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Further evidence that mechanisms of host/symbiont integration are dissimilar in the maternal versus embryonic Acyrthosiphon pisum bacteriome

EvoDevo ◽

10.1186/s13227-020-00168-5 ◽

2020 ◽

Vol 11 (1) ◽

Author(s):

Celeste R. Banfill ◽

Alex C. C. Wilson ◽

Hsiao-ling Lu

Keyword(s):

Amino Acids ◽

Amino Acid ◽

Acyrthosiphon Pisum ◽

Essential Amino Acids ◽

Developmental Time ◽

Follicular Epithelium ◽

Future Research ◽

Buchnera Aphidicola ◽

Bacterial Endosymbionts ◽

Asexual Embryogenesis

Abstract Background Host/symbiont integration is a signature of evolutionarily ancient, obligate endosymbioses. However, little is known about the cellular and developmental mechanisms of host/symbiont integration at the molecular level. Many insects possess obligate bacterial endosymbionts that provide essential nutrients. To advance understanding of the developmental and metabolic integration of hosts and endosymbionts, we track the localization of a non-essential amino acid transporter, ApNEAAT1, across asexual embryogenesis in the aphid, Acyrthosiphon pisum. Previous work in adult bacteriomes revealed that ApNEAAT1 functions to exchange non-essential amino acids at the A. pisum/Buchnera aphidicola symbiotic interface. Driven by amino acid concentration gradients, ApNEAAT1 moves proline, serine, and alanine from A. pisum to Buchnera and cysteine from Buchnera to A. pisum. Here, we test the hypothesis that ApNEAAT1 is localized to the symbiotic interface during asexual embryogenesis. Results During A. pisum asexual embryogenesis, ApNEAAT1 does not localize to the symbiotic interface. We observed ApNEAAT1 localization to the maternal follicular epithelium, the germline, and, in late-stage embryos, to anterior neural structures and insect immune cells (hemocytes). We predict that ApNEAAT1 provisions non-essential amino acids to developing oocytes and embryos, as well as to the brain and related neural structures. Additionally, ApNEAAT1 may perform roles related to host immunity. Conclusions Our work provides further evidence that the embryonic and adult bacteriomes of asexual A. pisum are not equivalent. Future research is needed to elucidate the developmental time point at which the bacteriome reaches maturity.

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Aphids evolved novel secreted proteins for symbiosis with bacterial endosymbiont

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2012.1952 ◽

2013 ◽

Vol 280 (1750) ◽

pp. 20121952 ◽

Cited By ~ 54

Author(s):

Shuji Shigenobu ◽

David L. Stern

Keyword(s):

Acyrthosiphon Pisum ◽

Developmental Time ◽

Secreted Proteins ◽

Buchnera Aphidicola ◽

Orphan Genes ◽

Specific Expression ◽

Small Proteins ◽

Endosymbiotic Bacteria ◽

Host Aphid

Aphids evolved novel cells, called bacteriocytes, that differentiate specifically to harbour the obligatory mutualistic endosymbiotic bacteria Buchnera aphidicola . The genome of the host aphid Acyrthosiphon pisum contains many orphan genes that display no similarity with genes found in other sequenced organisms, prompting us to hypothesize that some of these orphan genes are related to lineage-specific traits, such as symbiosis. We conducted deep sequencing of bacteriocytes mRNA followed by whole mount in situ hybridizations of over-represented transcripts encoding aphid-specific orphan proteins. We identified a novel class of genes that encode small proteins with signal peptides, which are often cysteine-rich, that are over-represented in bacteriocytes. These genes are first expressed at a developmental time point coincident with the incorporation of symbionts strictly in the cells that contribute to the bacteriocyte and this bacteriocyte-specific expression is maintained throughout the aphid's life. The expression pattern suggests that recently evolved secretion proteins act within bacteriocytes, perhaps to mediate the symbiosis with beneficial bacterial partners, which is reminiscent of the evolution of novel cysteine-rich secreted proteins of leguminous plants that regulate nitrogen-fixing endosymbionts.

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Population genetics: the next stop for microbial ecologists?

Open Life Sciences ◽

10.2478/s11535-011-0086-9 ◽

2011 ◽

Vol 6 (6) ◽

pp. 887-892 ◽

Cited By ~ 1

Author(s):

Ramiro Logares

Keyword(s):

Population Genetics ◽

High Throughput Sequencing ◽

Evolutionary Dynamics ◽

Biological Species ◽

Microbial Populations ◽

Clear Understanding ◽

Population Sizes ◽

Reproductive Rates ◽

Multicellular Organisms ◽

Shed Light

AbstractMicrobes play key roles in the functioning of the biosphere. Still, our knowledge about their total diversity is very limited. In particular, we lack a clear understanding of the evolutionary dynamics occurring within their populations (i.e. among members of the same biological species). Unlike animals and plants, microbes normally have huge population sizes, high reproductive rates and the potential for unrestricted dispersal. As a consequence, the knowledge of population genetics acquired from studying animals and plants cannot be applied without extensive testing to microbes. Next generation molecular tools, like High Throughput Sequencing (e.g. 454 and Illumina) coupled to Single Cell Genomics, now allow investigating microbial populations at a very fine scale. Such techniques have the potential to shed light on several ecological and evolutionary processes occurring within microbial populations that so far have remained hidden. Furthermore, they may facilitate the identification of microbial species. Eventually, we may find an answer to the question of whether microbes and multicellular organisms follow the same or different rules in their population diversification patterns.

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STRUCTURE AND DYNAMICS OF ENVIRONMENTAL PARAMETERS OF HUMAN INTESTINAL MICROBIOME IN DIFFERENT CLIMATIC AND ECOLOGICAL ZONES OF ST. PETERSBURG

Bulletin Biomedicine and sociology ◽

10.26787/nydha-2618-8783-2020-5-4-31-36 ◽

2020 ◽

pp. 31-36

Author(s):

Bugero N.V. ◽

Ilyina N.A. ◽

Aleksandrova S.M.

Keyword(s):

Environmental Parameters ◽

Intestinal Microbiome ◽

Ecological Niches ◽

Horizontal Structure ◽

Ecological Zones ◽

Qualitative And Quantitative ◽

Symbiotic Relationships ◽

Structure And Dynamics ◽

Quantitative Changes ◽

Micro Organisms

In order to understand the structure and dynamics of symbiotic relationships of human intestinal biotope micro-organisms, taxonomic constancy indices, the degree of contagion of the biocenosis under study and floristic significance were investigated, which made it possible to detect qualitative and quantitative changes in the microecology of the biotope being studied in persons living in different ecologically heterogeneous territories of Saint Petersburg. The contagiosity index estimated the distribution of species in space. Persons living in the ecologically disadvantaged Kirov district of the city have been found to show a reliable increase in this indicator for the obligate microflora: bifido and lacto bacteria, intestinal columns and bacteroids, compared to the resort district, which is considered a relatively favourable area for residence. On the contrary, there has been a reliable decrease in this indicator in the group of opportunistic micro-organisms (fungi of the genus Candida, staphylococcus, clostridium, etc.), resulting in the liberation of ecological niches successfully occupied by transient flora. This ratio reveals an imbalance of participation in the horizontal structure of the intestine ecosystem of the main symbiotes and representatives of the transient flora. To analyse the structure of symbiotic relationships, the constancy indices that form the microflora of the individuals of the groups studied were investigated. The analysis of the data obtained suggested that the dominant species in both groups were optional-anaerobic bifido and lactobacteria and oblique-anaerobic bacteroids. It should be noted, however, that in the residents of the dysfunctional Kirovsky district, against the background of the reduced constancy of the normal flora, opportunistic micro-organisms have entered. The floral significance index was also declining in the obligate flora of this group and increased for opportunistic species. Thus, the study of the environmental characteristics of the intestinal biotope using different ecological parameters for persons living in different technogenic load regions of St. Petersburg has shown that in the Kirov district with an unfavourable environmental situation there are compensated qualitative and quantitative changes in the intestinal microbiocenosis, resulting in a change in the hierarchy in the overall structure of micro-organisms.

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Matching the supply of bacterial nutrients to the nutritional demand of the animal host

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2014.1163 ◽

2014 ◽

Vol 281 (1791) ◽

pp. 20141163 ◽

Cited By ~ 32

Author(s):

Calum W. Russell ◽

Anton Poliakov ◽

Meena Haribal ◽

Georg Jander ◽

Klaas J. van Wijk ◽

...

Keyword(s):

Quantitative Proteomics ◽

Acyrthosiphon Pisum ◽

Feedback Inhibition ◽

Essential Amino Acids ◽

Host Cells ◽

Host Proteins ◽

Buchnera Aphidicola ◽

Symbiotic Microorganisms ◽

Precursor Supply ◽

Host Regulation

Various animals derive nutrients from symbiotic microorganisms with much-reduced genomes, but it is unknown whether, and how, the supply of these nutrients is regulated. Here, we demonstrate that the production of essential amino acids (EAAs) by the bacterium Buchnera aphidicola in the pea aphid Acyrthosiphon pisum is elevated when aphids are reared on diets from which that EAA are omitted, demonstrating that Buchnera scale EAA production to host demand. Quantitative proteomics of bacteriocytes (host cells bearing Buchnera ) revealed that these metabolic changes are not accompanied by significant change in Buchnera or host proteins, suggesting that EAA production is regulated post-translationally. Bacteriocytes in aphids reared on diet lacking the EAA methionine had elevated concentrations of both methionine and the precursor cystathionine, indicating that methionine production is promoted by precursor supply and is not subject to feedback inhibition by methionine. Furthermore, methionine production by isolated Buchnera increased with increasing cystathionine concentration. We propose that Buchnera metabolism is poised for EAA production at certain maximal rates, and the realized release rate is determined by precursor supply from the host. The incidence of host regulation of symbiont nutritional function via supply of key nutritional inputs in other symbioses remains to be investigated.

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Adaptation limits ecological diversification and promotes ecological tinkering during the competition for substitutable resources

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1807530115 ◽

2018 ◽

Vol 115 (44) ◽

pp. E10407-E10416 ◽

Cited By ~ 10

Author(s):

Benjamin H. Good ◽

Stephen Martis ◽

Oskar Hallatschek

Keyword(s):

Evolutionary Dynamics ◽

Competitive Exclusion ◽

Directional Selection ◽

Ecological Niches ◽

Ecological Diversification ◽

Effective Competition ◽

Uptake Rates ◽

Wide Range ◽

Dynamical Features ◽

Adaptation Limits

Microbial communities can evade competitive exclusion by diversifying into distinct ecological niches. This spontaneous diversification often occurs amid a backdrop of directional selection on other microbial traits, where competitive exclusion would normally apply. Yet despite their empirical relevance, little is known about how diversification and directional selection combine to determine the ecological and evolutionary dynamics within a community. To address this gap, we introduce a simple, empirically motivated model of eco-evolutionary feedback based on the competition for substitutable resources. Individuals acquire heritable mutations that alter resource uptake rates, either by shifting metabolic effort between resources or by increasing the overall growth rate. While these constitutively beneficial mutations are trivially favored to invade, we show that the accumulated fitness differences can dramatically influence the ecological structure and evolutionary dynamics that emerge within the community. Competition between ecological diversification and ongoing fitness evolution leads to a state of diversification–selection balance, in which the number of extant ecotypes can be pinned below the maximum capacity of the ecosystem, while the ecotype frequencies and genealogies are constantly in flux. Interestingly, we find that fitness differences generate emergent selection pressures to shift metabolic effort toward resources with lower effective competition, even in saturated ecosystems. We argue that similar dynamical features should emerge in a wide range of models with a mixture of directional and diversifying selection.

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Evolution to alternative levels of stable diversity leaves areas of niche space unexplored

10.1101/2021.01.06.425548 ◽

2021 ◽

Author(s):

Ilan N. Rubin ◽

Iaroslav Ispolatov ◽

Michael Doebeli

Keyword(s):

Evolutionary Dynamics ◽

Natural Populations ◽

Metastable States ◽

Community Diversity ◽

Limited Resources ◽

Niche Space ◽

Stable States ◽

Low Diversity ◽

Population Sizes ◽

Adaptive Radiations

AbstractOne of the oldest and most persistent questions in ecology and evolution is whether natural communities tend to evolve toward saturation and maximal diversity. Robert MacArthur’s classical theory of niche packing and the theory of adaptive radiations both imply that populations will diversify and fully partition any available niche space. However, the saturation of natural populations is still very much an open area of debate and investigation. Additionally, recent evolutionary theory suggests the existence of alternative evolutionary stable states (ESSs), which implies that some stable communities may not be fully saturated. Using models with classical Lokta-Volterra ecological dynamics and three formulations of evolutionary dynamics (a model using adaptive dynamics, an individual-based model, and a partial differential equation model), we show that following an adaptive radiation, communities can often get stuck in low diversity states when limited by mutations of small phenotypic effect. These low diversity metastable states can also be maintained by limited resources and finite population sizes. When small mutations and finite populations are considered together, it is clear that despite the presence of higher-diversity stable states, natural populations are likely not fully saturating their environment and leaving potential niche space unfilled. Additionally, within-species variation can further reduce community diversity from levels predicted by models that assume species-level homogeneity.Author summaryUnderstanding if and when communities evolve to saturate their local environments is imperative to our understanding of natural populations. Using computer simulations of classical evolutionary models, we study whether adaptive radiations tend to lead toward saturated communities in which no new species can invade or remain trapped in alternative, lower diversity stable states. We show that with asymmetric competition and small effect mutations, evolutionary Red Queen dynamics can trap communities in low diversity metastable states. Moreover, limited resources not only reduces community population sizes, but also reduces community diversity, denying the formation of saturated communities and stabilizing low diversity, non-stationary evolutionary dynamics. Our results are directly relevant to the longstanding questions important to both ecological empiricists and theoreticians on the species packing and saturation of natural environments. Also, by showing the ease evolution can trap communities in low diversity metastable stats, we demonstrate the potential harm in relying solely on ESSs to answer questions of biodiversity.

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Polygenic local adaptation in metapopulations: a stochastic eco-evolutionary model

10.1101/2020.06.16.154245 ◽

2020 ◽

Author(s):

Enikő Szép ◽

Himani Sachdeva ◽

Nick Barton

Keyword(s):

Population Size ◽

Local Adaptation ◽

Genetic Drift ◽

Diffusion Approximation ◽

Joint Distribution ◽

Evolutionary Model ◽

Ecological Niches ◽

Demographic Stochasticity ◽

Linkage Disequilibria ◽

Population Sizes

AbstractThis paper analyses the conditions for local adaptation in a metapopulation with infinitely many islands under a model of hard selection, where population size depends on local fitness. Each island belongs to one of two distinct ecological niches or habitats. Fitness is influenced by an additive trait which is under habitat-dependent directional selection. Our analysis is based on the diffusion approximation and accounts for both genetic drift and demographic stochasticity. By neglecting linkage disequilibria, it yields the joint distribution of allele frequencies and population size on each island. We find that under hard selection, the conditions for local adaptation in a rare habitat are more restrictive for more polygenic traits: even moderate migration load per locus at very many loci is sufficient for population sizes to decline. This further reduces the efficacy of selection at individual loci due to increased drift and because smaller populations are more prone to swamping due to migration, causing a positive feedback between increasing maladaptation and declining population sizes. Our analysis also highlights the importance of demographic stochasticity, which exacerbates the decline in numbers of maladapted populations, leading to population collapse in the rare habitat at significantly lower migration than predicted by deterministic arguments.

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Janthinobacterium CG23_2: Comparative Genome Analysis Reveals Enhanced Environmental Sensing and Transcriptional Regulation for Adaptation to Life in an Antarctic Supraglacial Stream

Microorganisms ◽

10.3390/microorganisms7100454 ◽

2019 ◽

Vol 7 (10) ◽

pp. 454

Author(s):

Markus Dieser ◽

Heidi J. Smith ◽

Thiruvarangan Ramaraj ◽

Christine M. Foreman

Keyword(s):

Transcriptional Regulation ◽

Extreme Environment ◽

Ecological Niches ◽

Genome Plasticity ◽

Functional Categories ◽

Environmental Sensing ◽

Copy Numbers ◽

Environmental Extremes ◽

Species Specific ◽

Extracellular Environment

As many bacteria detected in Antarctic environments are neither true psychrophiles nor endemic species, their proliferation in spite of environmental extremes gives rise to genome adaptations. Janthinobacterium sp. CG23_2 is a bacterial isolate from the Cotton Glacier stream, Antarctica. To understand how Janthinobacterium sp. CG23_2 has adapted to its environment, we investigated its genomic traits in comparison to genomes of 35 published Janthinobacterium species. While we hypothesized that genome shrinkage and specialization to narrow ecological niches would be energetically favorable for dwelling in an ephemeral Antarctic stream, the genome of Janthinobacterium sp. CG23_2 was on average 1.7 ± 0.6 Mb larger and predicted 1411 ± 499 more coding sequences compared to the other Janthinobacterium spp. Putatively identified horizontal gene transfer events contributed 0.92 Mb to the genome size expansion of Janthinobacterium sp. CG23_2. Genes with high copy numbers in the species-specific accessory genome of Janthinobacterium sp. CG23_2 were associated with environmental sensing, locomotion, response and transcriptional regulation, stress response, and mobile elements—functional categories which also showed molecular adaptation to cold. Our data suggest that genome plasticity and the abundant complementary genes for sensing and responding to the extracellular environment supported the adaptation of Janthinobacterium sp. CG23_2 to this extreme environment.

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Disentangling Complex Inheritance Patterns of Plant Organellar Genomes: An Example From Carrot

Journal of Heredity ◽

10.1093/jhered/esaa037 ◽

2020 ◽

Vol 111 (6) ◽

pp. 531-538 ◽

Cited By ~ 1

Author(s):

Jennifer R Mandel ◽

Adam J Ramsey ◽

Jacob M Holley ◽

Victoria A Scott ◽

Dviti Mody ◽

...

Keyword(s):

Evolutionary Dynamics ◽

Plant Mitochondria ◽

Special Focus ◽

Inheritance Patterns ◽

Daucus Carota L ◽

Organellar Genomes ◽

Complex Inheritance ◽

Plastid Markers ◽

Genome Information ◽

Experimental Crosses

Abstract Plant mitochondria and plastids display an array of inheritance patterns and varying levels of heteroplasmy, where individuals harbor more than 1 version of a mitochondrial or plastid genome. Organelle inheritance in plants has the potential to be quite complex and can vary with plant growth, development, and reproduction. Few studies have sought to investigate these complicated patterns of within-individual variation and inheritance using experimental crosses in plants. We carried out crosses in carrot, Daucus carota L. (Apiaceae), which has previously been shown to exhibit organellar heteroplasmy. We used mitochondrial and plastid markers to begin to disentangle the patterns of organellar inheritance and the fate of heteroplasmic variation, with special focus on cases where the mother displayed heteroplasmy. We also investigated heteroplasmy across the plant, assaying leaf samples at different development stages and ages. Mitochondrial and plastid paternal leakage was rare and offspring received remarkably similar heteroplasmic mixtures to their heteroplasmic mothers, indicating that heteroplasmy is maintained over the course of maternal inheritance. When offspring did differ from their mother, they were likely to exhibit a loss of the genetic variation that was present in their mother. Finally, we found that mitochondrial variation did not vary significantly over plant development, indicating that substantial vegetative sorting did not occur. Our study is one of the first to quantitatively investigate inheritance patterns and heteroplasmy in plants using controlled crosses, and we look forward to future studies making use of whole genome information to study the complex evolutionary dynamics of plant organellar genomes.

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