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      Long-Term Temperature Stress in the Coral Model Aiptasia Supports the “Anna Karenina Principle” for Bacterial Microbiomes

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          Abstract

          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.

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          Comparative Analysis of Human Gut Microbiota by Barcoded Pyrosequencing

          Humans host complex microbial communities believed to contribute to health maintenance and, when in imbalance, to the development of diseases. Determining the microbial composition in patients and healthy controls may thus provide novel therapeutic targets. For this purpose, high-throughput, cost-effective methods for microbiota characterization are needed. We have employed 454-pyrosequencing of a hyper-variable region of the 16S rRNA gene in combination with sample-specific barcode sequences which enables parallel in-depth analysis of hundreds of samples with limited sample processing. In silico modeling demonstrated that the method correctly describes microbial communities down to phylotypes below the genus level. Here we applied the technique to analyze microbial communities in throat, stomach and fecal samples. Our results demonstrate the applicability of barcoded pyrosequencing as a high-throughput method for comparative microbial ecology.
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            Correlation detection strategies in microbial data sets vary widely in sensitivity and precision.

            Disruption of healthy microbial communities has been linked to numerous diseases, yet microbial interactions are little understood. This is due in part to the large number of bacteria, and the much larger number of interactions (easily in the millions), making experimental investigation very difficult at best and necessitating the nascent field of computational exploration through microbial correlation networks. We benchmark the performance of eight correlation techniques on simulated and real data in response to challenges specific to microbiome studies: fractional sampling of ribosomal RNA sequences, uneven sampling depths, rare microbes and a high proportion of zero counts. Also tested is the ability to distinguish signals from noise, and detect a range of ecological and time-series relationships. Finally, we provide specific recommendations for correlation technique usage. Although some methods perform better than others, there is still considerable need for improvement in current techniques.
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              The genome of Aiptasia, a sea anemone model for coral symbiosis.

              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.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                08 May 2019
                2019
                : 10
                : 975
                Affiliations
                Division of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology , Thuwal, Saudi Arabia
                Author notes

                Edited by: George Tsiamis, University of Patras, Greece

                Reviewed by: Julie L. Meyer, University of Florida, United States; Mauricio Rodriguez-Lanetty, Florida International University, United States

                *Correspondence: Manuel Aranda, manuel.aranda@ 123456kaust.edu.sa

                These authors have contributed equally to this work

                Present address: Yi Jin Liew, CSIRO Health and Biosecurity, North Ryde, NSW, Australia

                This article was submitted to Systems Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.00975
                6517863
                31139158
                c806c67e-2dbf-4869-b3a4-669c3328fc7e
                Copyright © 2019 Ahmed, Herrera, Liew and Aranda.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 17 December 2018
                : 18 April 2019
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 102, Pages: 11, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                β-diversity,dispersion,microbiome,16s rrna gene,temperature
                Microbiology & Virology
                β-diversity, dispersion, microbiome, 16s rrna gene, temperature

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