Erratum: Long-Term Temperature Stress in the Coral Model Aiptasia Supports the "Anna Karenina Principle" for Bacterial Microbiomes.
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SUBMITTER: Frontiers Production Office
PROVIDER: S-EPMC6657528 | biostudies-literature | 2019
REPOSITORIES: biostudies-literature
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Erratum: Long-Term Temperature Stress in the Coral Model Aiptasia Supports the "Anna Karenina Principle" for Bacterial Microbiomes.
Frontiers in microbiology 20190718
[This corrects the article DOI: 10.3389/fmicb.2019.00975.]. ...[more]
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Project description:The understanding of host-microbial partnerships has become a hot topic during the last decade as it has been shown that associated microbiota play critical roles in the host physiological functions and susceptibility to diseases. Moreover, the microbiome may contribute to host resilience to environmental stressors. The sea anemone Aiptasia is a good laboratory model system to study corals and their microbial symbiosis. In this regard, studying its bacterial microbiota provides a better understanding of cnidarian metaorganisms as a whole. Here, we investigated the bacterial communities of different Aiptasia host-symbiont combinations under long-term heat stress in laboratory conditions. Following a 16S rRNA gene sequencing approach we were able to detect significant differences in the bacterial composition and structure of Aiptasia reared at different temperatures. A higher number of taxa (i.e., species richness), and consequently increased α-diversity and β-dispersion, were observed in the microbiomes of heat-stressed individuals across all host strains and experimental batches. Our findings are in line with the recently proposed Anna Karenina principle (AKP) for animal microbiomes, which states that dysbiotic or stressed organisms have a more variable and unstable microbiome than healthy ones. Microbial interactions affect the fitness and survival of their hosts, thus exploring the AKP effect on animal microbiomes is important to understand host resilience. Our data contributes to the current knowledge of the Aiptasia holobiont and to the growing field of study of host-associated microbiomes.
| S-EPMC6517863 | biostudies-literature
Project description:The AKP (Anna Karenina principle), which refers to observations inspired by the opening line of Leo Tolstoy's Anna Karenina, "all happy families are all alike; each unhappy family is unhappy in its own way," predicts that all "healthy" microbiomes are alike and each disease-associated microbiome is "sick" in its own way in human microbiome-associated diseases (MADs). The AKP hypothesis predicts the rise of heterogeneity/stochasticity in human microbiomes associated with dysbiosis due to MADs. We used the beta-diversity in Hill numbers and stochasticity analysis to detect AKP and anti-AKP effects. We tested the AKP with 27 human MAD studies and discovered that the AKP, anti-AKP, and non-AKP effects were exhibited in approximately 50%, 25%, and 25% of the MAD cases, respectively. Mechanistically, AKP effects are primarily influenced by highly dominant microbial species and less influenced by rare species. In contrast, all species appear to play equal roles in influencing anti-AKP effects.
| S-EPMC7163324 | biostudies-literature
Project description:BackgroundAlthough localized aggressive periodontitis (LAP), generalized aggressive periodontitis (GAP), and chronic periodontitis (CP) are microbially driven diseases, our inability to separate disease-specific associations from those common to all three forms of periodontitis has hampered biomarker discovery. Therefore, we aimed to map the genomic content of, and the biological pathways encoded by, the microbiomes associated with these clinical phenotypes. We also estimated the extent to which these biomes are governed by the Anna Karenina principle (AKP), which states that eubiotic communities are similar between individuals while disease-associated communities are highly individualized.MethodsWe collected subgingival plaque from 25 periodontally healthy individuals and diseased sites of 59 subjects with stage 3 periodontitis and used shotgun metagenomics to characterize the aggregate of bacterial genes.ResultsBeta-dispersion metrics demonstrated that AKP was most evident in CP, followed by GAP and LAP. We discovered broad dysbiotic signatures spanning the three phenotypes, with over-representation of pathways that facilitate life in an oxygen-poor, protein- and heme-rich, pro-oxidant environment and enhance capacity for attachment and biofilm formation. Phenotype-specific indicators were more readily evident in LAP microbiome than GAP or CP. Genes that enable acetate-scavenging lifestyle, utilization of alternative nutritional sources, oxidative and nitrosative stress responses, and siderophore production were unique to LAP. An attenuation of virulence-related functionalities and stress response from LAP to GAP to CP was apparent. We also discovered that clinical phenotypes of disease resolved variance in the microbiome with greater clarity than the newly established grading system. Importantly, we observed that one third of the metagenome of LAP is unique to this phenotype while GAP shares significant functional and taxonomic features with both LAP and CP, suggesting either attenuation of an aggressive disease or an early-onset chronic disease.ConclusionWithin the limitations of a small sample size and a cross-sectional study design, the distinctive features of the microbiomes associated with LAP and CP strongly persuade us that these are discrete disease entities, while calling into question whether GAP is a separate disease, or an artifact induced by cross-sectional study designs. Further studies on phenotype-specific microbial genes are warranted to explicate their role in disease etiology. Video Abstract.
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Project description:Gut microbial communities are critical in determining the evolutive success of fruit fly phytophagous pests (Diptera, Tephritidae), facilitating their adaptation to suboptimal environmental conditions and to plant allelochemical defences. An important source of variation for the microbial diversity of fruit flies is represented by the crop on which larvae are feeding. However, a "crop effect" is not always the main driver of microbial patterns, and it is often observed in combination with other and less obvious processes. In this work, we aim at verifying if environmental stress and, by extension, changing environmental conditions, can promote microbial diversity in Zeugodacus cucurbitae (Coquillett), a cosmopolitan pest of cucurbit crops. With this objective, 16S rRNA metabarcoding was used to test differences in the microbial profiles of wild fly populations in a large experimental setup in Eastern Central Tanzania. The analysis of 2,973 unique ASV, which were assigned to 22 bacterial phyla, 221 families and 590 putative genera, show that microbial α diversity (as estimated by Abundance Coverage Estimator, Faith's Phylogenetic Diversity, Shannon-Weiner and the Inverse Simpson indexes) as well as β microbial diversity (as estimated by Compositional Data analysis of ASVs and of aggregated genera) significantly change as the species gets closer to its altitudinal limits, in farms where pesticides and agrochemicals are used. Most importantly, the multivariate dispersion of microbial patterns is significantly higher in these stressful environmental conditions thus indicating that Anna Karenina effects contribute to the microbial diversity of Z. cucurbitae. The crop effect was comparably weaker and detected as non-consistent changes across the experimental sites. We speculate that the impressive adaptive potential of polyphagous fruit flies is, at least in part, related to the Anna Karenina principle, which promotes stochastic changes in the microbial diversity of fly populations exposed to suboptimal environmental conditions.
| S-EPMC10990204 | biostudies-literature
Project description:The coral-algal symbiosis is maintained by a constant and limited nitrogen availability in the holobiont. Denitrifiers, i.e., prokaryotes reducing nitrate/nitrite to dinitrogen, could contribute to maintaining the nitrogen limitation in the coral holobiont, however the effect of host and algal identity on their community is still unknown. Using the coral model Aiptasia, we quantified and characterized the denitrifier community in a full-factorial design combining two hosts (CC7 and H2) and two strains of algal symbionts of the family Symbiodiniaceae (SSA01 and SSB01). Strikingly, relative abundance of denitrifiers increased by up to 22-fold in photosymbiotic Aiptasia compared to their aposymbiotic (i.e., algal-depleted) counterparts. In line with this, while the denitrifier community in aposymbiotic Aiptasia was largely dominated by diet-associated Halomonas, we observed an increasing relative abundance of an unclassified bacterium in photosymbiotic CC7, and Ketobacter in photosymbiotic H2, respectively. Pronounced changes in denitrifier communities of Aiptasia with Symbiodinium linucheae strain SSA01 aligned with the higher photosynthetic carbon availability of these holobionts compared to Aiptasia with Breviolum minutum strain SSB01. Our results reveal that the presence of algal symbionts increases abundance and alters community structure of denitrifiers in Aiptasia. Thereby, patterns in denitrifier community likely reflect the nutritional status of aposymbiotic vs. symbiotic holobionts. Such a passive regulation of denitrifiers may contribute to maintaining the nitrogen limitation required for the functioning of the cnidarian-algal symbiosis.
| S-EPMC9723753 | biostudies-literature
Project description:The endosymbiosis between dinoflagellate algae of the genus Symbiodinium and stony corals provides the foundation of coral reef ecosystems. Coral bleaching, the expulsion of endosymbionts from the coral host tissue as a consequence of heat or light stress, poses a threat to reef ecosystem functioning on a global scale. Hence, a better understanding of the factors contributing to heat stress susceptibility and tolerance is needed. In this regard, some of the most thermotolerant corals live in particularly saline habitats, but possible effects of high salinity on thermotolerance in corals are anecdotal. Here we test the hypothesis that high salinity may lead to increased thermotolerance. We conducted a heat stress experiment at low, intermediate, and high salinities using a set of host-endosymbiont combinations of the coral model Aiptasia. As expected, all host-endosymbiont combinations showed reduced photosynthetic efficiency and endosymbiont loss during heat stress, but the severity of bleaching was significantly reduced with increasing salinities for one of the host-endosymbiont combinations. Our results show that higher salinities can convey increased thermotolerance in Aiptasia, although this effect seems to be dependent on the particular host strain and/or associated symbiont type. This finding may help explain the extraordinarily high thermotolerance of corals in high salinity environments, such as the Red Sea and the Persian/Arabian Gulf, and provides novel insight regarding factors that contribute to thermotolerance. Since our results are based on a salinity effect in symbiotic sea anemones, it remains to be determined whether this salinity effect can also be observed in stony corals.
| S-EPMC5769654 | biostudies-literature
Project description:Aiptasia is an emerging model organism to study cnidarian symbioses due to its taxonomic relatedness to other anthozoans such as stony corals and similarities of its microalgal and bacterial partners, complementing the existing Hydra (Hydrozoa) and Nematostella (Anthozoa) model systems. Despite the availability of studies characterizing the microbiomes of several natural Aiptasia populations and laboratory strains, knowledge on basic information, such as surface topography, bacterial carrying capacity, or the prospect of microbiome manipulation is lacking. Here we address these knowledge gaps. Our results show that the surface topographies of the model hydrozoan Hydra and anthozoans differ substantially, whereas the ultrastructural surface architecture of Aiptasia and stony corals is highly similar. Further, we determined a bacterial carrying capacity of ∼104 and ∼105 bacteria (i.e., colony forming units, CFUs) per polyp for aposymbiotic and symbiotic Aiptasia anemones, respectively, suggesting that the symbiotic status changes bacterial association/density. Microbiome transplants from Acropora humilis and Porites sp. to gnotobiotic Aiptasia showed that only a few foreign bacterial taxa were effective colonizers. Our results shed light on the putative difficulties of transplanting microbiomes between cnidarians in a manner that consistently changes microbial host association at large. At the same time, our study provides an avenue to identify bacterial taxa that exhibit broad ability to colonize different hosts as a starting point for cross-species microbiome manipulation. Our work is relevant in the context of microbial therapy (probiotics) and microbiome manipulation in corals and answers to the need of having cnidarian model systems to test the function of bacteria and their effect on holobiont biology. Taken together, we provide important foundation data to extend Aiptasia as a coral model for bacterial functional studies.
| S-EPMC8060496 | biostudies-literature
Project description:Evidence to date indicates that elevated seawater temperatures increase the occurrence of coral disease, which is frequently microbial in origin. Microbial behaviors such as motility and chemotaxis are often implicated in coral colonization and infection, yet little is known about the effect of warming temperatures on these behaviors. Here we present data demonstrating that increasing water temperatures induce two behavioral switches in the coral pathogen Vibrio coralliilyticus that considerably augment the bacterium's performance in tracking the chemical signals of its coral host, Pocillopora damicornis. Coupling field-based heat-stress manipulations with laboratory-based observations in microfluidic devices, we recorded the swimming behavior of thousands of individual pathogen cells at different temperatures, associated with current and future climate scenarios. When temperature reached ?23?°C, we found that the pathogen's chemotactic ability toward coral mucus increased by >60%, denoting an enhanced capability to track host-derived chemical cues. Raising the temperature further, to 30?°C, increased the pathogen's chemokinetic ability by >57%, denoting an enhanced capability of cells to accelerate in favorable, mucus-rich chemical conditions. This work demonstrates that increasing temperature can have strong, multifarious effects that enhance the motile behaviors and host-seeking efficiency of a marine bacterial pathogen.
| S-EPMC5029190 | biostudies-literature
Project description:The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between a cnidarian animal host (the coral) and intracellular photosynthetic dinoflagellate algae. The molecular and cellular mechanisms underlying this endosymbiosis are not well understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable laboratory model for investigating these mechanisms. Here we report on the assembly and analysis of the Aiptasia genome, which will provide a foundation for future studies and has revealed several features that may be key to understanding the evolution and function of the endosymbiosis. These features include genomic rearrangements and taxonomically restricted genes that may be functionally related to the symbiosis, aspects of host dependence on alga-derived nutrients, a novel and expanded cnidarian-specific family of putative pattern-recognition receptors that might be involved in the animal-algal interactions, and extensive lineage-specific horizontal gene transfer. Extensive integration of genes of prokaryotic origin, including genes for antimicrobial peptides, presumably reflects an intimate association of the animal-algal pair also with its prokaryotic microbiome.
| S-EPMC4586855 | biostudies-literature
Project description:Coral microbiomes are known to play important roles in organismal health, response to environmental stress, and resistance to disease. The coral microbiome contains diverse assemblages of resident bacteria, ranging from defensive and metabolic symbionts to opportunistic bacteria that may turn harmful in compromised hosts. However, little is known about how these bacterial interactions influence the mechanism and controls of overall structure, stability, and function of the microbiome. We sought to test how coral microbiome dynamics were affected by interactions between two bacteria: Vibrio coralliilyticus, a known temperature-dependent pathogen of some corals, and Halobacteriovorax, a unique bacterial predator of Vibrio and other gram-negative bacteria. We challenged reef-building coral with V. coralliilyticus in the presence or absence of Halobacteriovorax predators, and monitored microbial community dynamics with 16S rRNA gene profiling time-series. Vibrio coralliilyticus inoculation increased the mean relative abundance of Vibrios by greater than 35% from the 4 to 8 hour time point, but not in the 24 & 32 hour time points. However, strong secondary effects of the Vibrio challenge were also observed for the rest of the microbiome such as increased richness (observed species), and reduced stability (increased beta-diversity). Moreover, after the transient increase in Vibrios, two lineages of bacteria (Rhodobacterales and Cytophagales) increased in coral tissues, suggesting that V. coralliilyticus challenge opens niche space for these known opportunists. Rhodobacterales increased from 6.99% (±0.05 SEM) to a maximum mean relative abundance of 48.75% (±0.14 SEM) in the final time point and Cytophagales from <0.001% to 3.656%. Halobacteriovorax predators are commonly present at low-abundance on coral surfaces. Based on the keystone role of predators in many ecosystems, we hypothesized that Halobacteriovorax predators might help protect corals by consuming foreign or "alien" gram negative bacteria. Halobacteriovorax inoculation also altered the microbiome but to a lesser degree than V. coralliilyticus, and Halobacteriovorax were never detected after inoculation. Simultaneous challenge with both V. coralliilyticus and predatory Halobacteriovorax eliminated the increase in V. coralliilyticus, ameliorated changes to the rest of the coral microbiome, and prevented the secondary blooms of opportunistic Rhodobacterales and Cytophagales seen in the V. coralliilyticus challenge. These data suggest that, under certain circumstances, host-associated bacterial predators may mitigate the ability of other bacteria to destabilize the microbiome.
| S-EPMC5455293 | biostudies-literature