Natural selection drives the fine-scale divergence of a coevolutionary arms race involving a long-mouthed weevil and its obligate host plant

<p>Abstract</p> <p>Background</p> <p>One of the major recent advances in evolutionary biology is the recognition that evolutionary interactions between species are substantially differentiated among geographic populations. To date, several authors have revealed natural selection pressures mediating the geographically-divergent processes of coevolution. How local, then, is the geographic structuring of natural selection in coevolutionary systems?</p> <p>Results</p> <p>I examined the spatial scale of a "geographic selection mosaic," focusing on a system involving a seed-predatory insect, the camellia weevil (<it>Curculio camelliae</it>), and its host plant, the Japanese camellia (<it>Camellia japonica</it>). In this system, female weevils excavate camellia fruits with their extremely-long mouthparts to lay eggs into seeds, while camellia seeds are protected by thick pericarps. Quantitative evaluation of natural selection demonstrated that thicker camellia pericarps are significantly favored in some, but not all, populations within a small island (Yakushima Island, Japan; diameter ca. 30 km). At the extreme, camellia populations separated by only several kilometers were subject to different selection pressures. Interestingly, in a population with the thickest pericarps, camellia individuals with intermediate pericarp thickness had relatively high fitness when the potential costs of producing thick pericarps were considered. Also importantly, some parameters of the weevil - camellia interaction such as the severity of seed infestation showed clines along temperature, suggesting the effects of climate on the fine-scale geographic differentiation of the coevolutionary processes.</p> <p>Conclusion</p> <p>These results show that natural selection can drive the geographic differentiation of interspecific interactions at surprisingly small spatial scales. Future studies should reveal the evolutionary/ecological outcomes of the "fine scale geographic mosaics" in biological communities.</p

Leaf-associated microbiomes of grafted tomato plants

Bacteria and fungi form complex communities (microbiomes) in above- and below-ground organs of plants, contributing to hosts’ growth and survival in various ways. Recent studies have suggested that host plant genotypes control, at least partly, plant-associated microbiome compositions. However, we still have limited knowledge of how microbiome structures are determined in/on grafted crop plants, whose above-ground (scion) and below-ground (rootstock) genotypes are different with each other. By using eight varieties of grafted tomato plants, we examined how rootstock genotypes could determine the assembly of leaf endophytic microbes in field conditions. An Illumina sequencing analysis showed that both bacterial and fungal community structures did not significantly differ among tomato plants with different rootstock genotypes: rather, sampling positions in the farmland contributed to microbiome variation in a major way. Nonetheless, a further analysis targeting respective microbial taxa suggested that some bacteria and fungi could be preferentially associated with particular rootstock treatments. Specifically, a bacterium in the genus Deinococcus was found disproportionately from ungrafted tomato individuals. In addition, yeasts in the genus Hannaella occurred frequently on the tomato individuals whose rootstock genotype was “Ganbarune”. Overall, this study suggests to what extent leaf microbiome structures can be affected/unaffected by rootstock genotypes in grafted crop plants

Deterministic and stochastic processes generating alternative states of microbiomes

微生物叢のゆらぎと安定性 --多種細菌群集の「代替状態」と制御可能性--. 京都大学プレスリリース. 2024-02-29.The structure of microbiomes is often classified into discrete or semi-discrete types potentially differing in community-scale functional profiles. Elucidating the mechanisms that generate such “alternative states” of microbiome compositions has been one of the major challenges in ecology and microbiology. In a time-series analysis of experimental microbiomes, we here show that both deterministic and stochastic ecological processes drive divergence of alternative microbiome states. We introduced species-rich soil-derived microbiomes into eight types of culture media with 48 replicates, monitoring shifts in community compositions at six time points (8 media × 48 replicates × 6 time points = 2304 community samples). We then confirmed that microbial community structure diverged into a few state types in each of the eight medium conditions as predicted in the presence of both deterministic and stochastic community processes. In other words, microbiome structure was differentiated into a small number of reproducible compositions under the same environment. This fact indicates not only the presence of selective forces leading to specific equilibria of community-scale resource use but also the influence of demographic drift (fluctuations) on the microbiome assembly. A reference-genome-based analysis further suggested that the observed alternative states differed in ecosystem-level functions. These findings will help us examine how microbiome structure and functions can be controlled by changing the “stability landscapes” of ecological community compositions

Interaction network rewiring and species’ contributions to community-scale flexibility

「やわらかい」ネットワークを作るコア生物種 --生態系の柔軟性を支える種を探索する--. 京都大学プレスリリース. 2024-03-07.The architecture of species interaction networks is a key factor determining the stability of ecological communities. However, the fact that ecological network architecture can change through time is often overlooked in discussions on community-level processes, despite its theoretical importance. By compiling a time-series community dataset involving 50 spider species and 974 Hexapoda prey species/strains, we quantified the extent to which the architecture of predator–prey interaction networks could shift across time points. We then developed a framework for finding species that could increase the flexibility of the interaction network architecture. Those “network coordinator” species are expected to promote the persistence of species-rich ecological communities by buffering perturbations in communities. Although spiders are often considered as generalist predators, their contributions to network flexibility vary greatly among species. We also found that detritivorous prey species can be cores of interaction rewiring, dynamically interlinking below-ground and above-ground community dynamics. We further found that the predator–prey interactions between those network coordinators differed from those highlighted in the standard network-analytical framework assuming static topology. Analyses of network coordinators will add a new dimension to our understanding of species coexistence mechanisms and provide platforms for systematically prioritizing species in terms of their potential contributions in ecosystem conservation and restoration

Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance

「1+1=2」じゃない共生の世界 --2種の菌が植物にもたらす相乗効果と相殺効果--. 京都大学プレスリリース. 2021-09-17.In natural and agricultural ecosystems, survival and growth of plants depend substantially on residing microbes in the endosphere and rhizosphere. Although numerous studies have reported the presence of plant-growth promoting bacteria and fungi in below-ground biomes, it remains a major challenge to understand how sets of microbial species positively or negatively affect plants’ performance. By conducting a series of single- and dual-inoculation experiments of 13 plant-associated fungi targeting a Brassicaceae plant species (Brassica rapa var. perviridis), we here systematically evaluated how microbial effects on plants depend on presence/absence of co-occurring microbes. The comparison of single- and dual-inoculation experiments showed that combinations of the fungal isolates with the highest plant-growth promoting effects in single inoculations did not have highly positive impacts on plant performance traits (e.g., shoot dry weight). In contrast, pairs of fungi with small/moderate contributions to plant growth in single-inoculation contexts showed the greatest effects on plants among the 78 fungal pairs examined. These results on the offset and synergistic effects of pairs of microbes suggest that inoculation experiments of single microbial species/isolates can result in the overestimation or underestimation of microbial functions in multi-species contexts. Because keeping single-microbe systems under outdoor conditions is impractical, designing sets of microbes that can maximize performance of crop plants is an important step for the use of microbial functions in sustainable agriculture

Leaf, root, and soil microbiomes of an invasive plant, Ardisia crenata, differ between its native and exotic ranges

IntroductionEcological underpinnings of the invasion success of exotic plants may be found in their interactions with microbes, either through the enemy release hypothesis and the enhanced mutualism hypothesis. Whereas recent high-throughput sequencing techniques have significantly expanded our understanding of plant-associated microbiomes and their functional guilds, few studies to date have used these techniques to compare the microbiome associated with invasive plants between their native and exotic ranges.MethodsWe extracted fungal and bacterial DNA within leaf endosphere, root endosphere and soil of an invasive plant, Ardisia crenata, sampled from their native range Japan and exotic range Florida, USA. Using Illumina sequencing data, we compared microbial community compositions and diversity between the native and exotic ranges, and tested whether abundance of pathogenic or mutualistic microbes differ between the native or exotic ranges in accordance to the enemy release hypothesis or the enhanced mutualism hypothesis.ResultsFungal and bacterial community compositions differed among leaves, roots and soil, and between the native and exotic ranges. Despite a higher microbial diversity in the soil in the exotic range than in the native range, the microbial diversity within leaf and root was lower in the exotic range compared to the native range. In addition, leaves in the native range harbored a greater number of plant pathogenic fungi compared to those in the exotic range.DiscussionThese patterns suggest plant controls over what microbes become associated with leaves and roots. The higher abundance of leaf pathogenic fungi, including the pathogen which is known to cause specific disease in A. crenata in the exotic range than in the native range, support the enemy release hypothesis and highlighted potential importance of examining microbial communities both above- and below-ground

Factors Influencing Leaf- and Root-Associated Communities of Bacteria and Fungi Across 33 Plant Orders in a Grassland

In terrestrial ecosystems, plants interact with diverse taxonomic groups of bacteria and fungi in the phyllosphere and rhizosphere. Although recent studies based on high-throughput DNA sequencing have drastically increased our understanding of plant-associated microbiomes, we still have limited knowledge of how plant species in a species-rich community differ in their leaf and root microbiome compositions. In a cool-temperate semi-natural grassland in Japan, we compared leaf- and root-associated microbiomes across 137 plant species belonging to 33 plant orders. Based on the whole-microbiome inventory data, we analyzed how sampling season as well as the taxonomy, nativeness (native or alien), lifeform (herbaceous or woody), and mycorrhizal type of host plants could contribute to variation in microbiome compositions among co-occurring plant species. The data also allowed us to explore prokaryote and fungal lineages showing preferences for specific host characteristics. The list of microbial taxa showing significant host preferences involved those potentially having some impacts on survival, growth, or environmental resistance of host plants. Overall, this study provides a platform for understanding how plant and microbial communities are linked with each other at the ecosystem level

Core species and interactions prominent in fish-associated microbiome dynamics

魚の健康において鍵となる「コア微生物叢」 --ウナギ養殖水槽内の細菌叢動態--. 京都大学プレスリリース. 2023-03-30.[Background] In aquatic ecosystems, the health and performance of fish depend greatly on the dynamics of microbial community structure in the background environment. Nonetheless, finding microbes with profound impacts on fish’s performance out of thousands of candidate species remains a major challenge. [Methods] We examined whether time-series analyses of microbial population dynamics could illuminate core components and structure of fish-associated microbiomes in the background (environmental) water. By targeting eel-aquaculture-tank microbiomes as model systems, we reconstructed the population dynamics of the 9605 bacterial and 303 archaeal species/strains across 128 days. [Results] Due to the remarkable increase/decrease of constituent microbial population densities, the taxonomic compositions of the microbiome changed drastically through time. We then found that some specific microbial taxa showed a positive relationship with eels’ activity levels even after excluding confounding effects of environmental parameters (pH and dissolved oxygen level) on population dynamics. In particular, a vitamin-B12-producing bacteria, Cetobacterium somerae, consistently showed strong positive associations with eels’ activity levels across the replicate time series of the five aquaculture tanks analyzed. Network theoretical and metabolic modeling analyses further suggested that the highlighted bacterium and some other closely-associated bacteria formed “core microbiomes” with potentially positive impacts on eels. [Conclusions] Overall, these results suggest that the integration of microbiology, ecological theory, and network science allows us to explore core species and interactions embedded within complex dynamics of fish-associated microbiomes

Below-ground plant-fungus network topology is not congruent with above-ground plant-animal network topology

植物を支える「共生ネットワーク」は地上と地下で構造が違う --見えてきた地下生物圏の構造--. 京都大学プレスリリース. 2015-10-26.In nature, plants and their pollinating and/or seed-dispersing animals form complex interaction networks. The commonly observed pattern of links between specialists and generalists in these networks has been predicted to promote species coexistence. Plants also build highly species-rich mutualistic networks below ground with root-associated fungi, and the structure of these plant–fungus networks may also affect terrestrial community processes. By compiling high-throughput DNA sequencing data sets of the symbiosis of plants and their root-associated fungi from three localities along a latitudinal gradient, we uncovered the entire network architecture of these interactions under contrasting environmental conditions. Each network included more than 30 plant species and hundreds of mycorrhizal and endophytic fungi belonging to diverse phylogenetic groups. The results were consistent with the notion that processes shaping host-plant specialization of fungal species generate a unique linkage pattern that strongly contrasts with the pattern of above-ground plant–partner networks. Specifically, plant–fungus networks lacked a “nested” architecture, which has been considered to promote species coexistence in plant–partner networks. Rather, the below-ground networks had a conspicuous “antinested” topology. Our findings lead to the working hypothesis that terrestrial plant community dynamics are likely determined by the balance between above-ground and below-ground webs of interspecific interactions

Bioactive polyamine production by a novel hybrid system comprising multiple indigenous gut bacterial strategies

個々の腸内細菌の生き残り戦略が組み合わさることで、 機能性物質ポリアミンが産生されていることを発見しました. 京都大学プレスリリース. 2018-07-06.Metabolites of the intestinal microbiota are thought to be generated through metabolic pathways spanning multiple taxa of intestinal bacteria. We have previously shown that the level of putrescine, a polyamine found abundantly in the human intestinal lumen, is increased in the colonic lumen following administration of arginine and the probiotic Bifidobacterium sp.; however, the underlying mechanism remained poorly understood. We report a novel pathway for putrescine production from arginine through agmatine involving the collaboration of two bacterial groups, and triggered by environmental acidification (drop in pH to below 6.5 from neutral). This pathway comprises the acid tolerance system of Escherichia coli, representing bacteria that have an arginine-dependent acid resistance system; the energy production system of Enterococcus faecalis, representing bacteria that have an agmatine deiminase system; and the acid production system of the acid-producing bacteria, represented by Bifidobacterium spp. This pathway is unique in that it represents a relationship between the independent survival strategies of multiple bacteria