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      The fecal microbiota from children with autism impact gut metabolism and learning and memory abilities of honeybees

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          Abstract

          Autism spectrum disorder (ASD) is a set of neurodevelopmental disorders, with an increasing incidence. Gastrointestinal symptoms are common comorbidities of ASD. The gut microbiota composition of children with autism is distinct from that of typical developmental (TD) children, suggesting that the gut microbiota probably influences on hosts via the microbiota-gut-brain axis. However, the relationship between intestinal dysbiosis and host brain function remains unclear. In this study, we creatively developed a honeybee model and investigated the potential effects of fecal microbiota on hosts. Fecal microbiota from children with autism and TD children were transplanted into microbiota-free honeybees ( Apis mellifera), resulting in induced ASD-fecal microbiota transplantation (FMT) honeybees (A-BEE group) and TD-FMT honeybees (T-BEE group), respectively. We found that cognitive abilities of honeybees in the A-BEE group were significantly impaired in olfactory proboscis extension response conditioning. Metagenomics was used to evaluate fecal microbiota colonization, revealing several differential species responsible for altered tryptophan metabolism and taurine metabolism within the bee gut, including Bacteroides dorei, Bacteroides fragilis, Lactobacillus gasseri, and Lactobacillus paragasseri. Furthermore, fecal microbiota from children with autism downregulated brain genes involved in neural signaling and synaptic transmission within honeybees. Notably, differentially spliced genes observed within brains of honeybees from the A-BEE group largely overlapped with those identified in human diagnosed with autism via SFARI and SPARK gene sets. These differentially spliced genes were also enriched within pathways related to neural synaptic transmission. Our findings provide novel insights into the pivotal role of the human gut microbiota, which may contribute to neurological processes in honeybees. Additionally, we present a few research sources on gut-brain connections in ASD.

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          Most cited references125

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          Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

          In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.
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            Cytoscape: a software environment for integrated models of biomolecular interaction networks.

            Cytoscape is an open source software project for integrating biomolecular interaction networks with high-throughput expression data and other molecular states into a unified conceptual framework. Although applicable to any system of molecular components and interactions, Cytoscape is most powerful when used in conjunction with large databases of protein-protein, protein-DNA, and genetic interactions that are increasingly available for humans and model organisms. Cytoscape's software Core provides basic functionality to layout and query the network; to visually integrate the network with expression profiles, phenotypes, and other molecular states; and to link the network to databases of functional annotations. The Core is extensible through a straightforward plug-in architecture, allowing rapid development of additional computational analyses and features. Several case studies of Cytoscape plug-ins are surveyed, including a search for interaction pathways correlating with changes in gene expression, a study of protein complexes involved in cellular recovery to DNA damage, inference of a combined physical/functional interaction network for Halobacterium, and an interface to detailed stochastic/kinetic gene regulatory models.
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              Basic local alignment search tool.

              A new approach to rapid sequence comparison, basic local alignment search tool (BLAST), directly approximates alignments that optimize a measure of local similarity, the maximal segment pair (MSP) score. Recent mathematical results on the stochastic properties of MSP scores allow an analysis of the performance of this method as well as the statistical significance of alignments it generates. The basic algorithm is simple and robust; it can be implemented in a number of ways and applied in a variety of contexts including straightforward DNA and protein sequence database searches, motif searches, gene identification searches, and in the analysis of multiple regions of similarity in long DNA sequences. In addition to its flexibility and tractability to mathematical analysis, BLAST is an order of magnitude faster than existing sequence comparison tools of comparable sensitivity.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/2390006/overviewRole: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/1251017/overviewRole: Role: Role:
                URI : https://loop.frontiersin.org/people/1167537/overviewRole: Role: Role:
                URI : https://loop.frontiersin.org/people/754226/overviewRole: Role: Role:
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                URI : https://loop.frontiersin.org/people/1564837/overviewRole: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/1246858/overviewRole: Role: Role: Role:
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                23 November 2023
                2023
                : 14
                : 1278162
                Affiliations
                [1] 1Microbiota Division, Department of Gastroenterology and Hepatology, First Medical Center, Chinese PLA General Hospital , Beijing, China
                [2] 2Medical School of Chinese PLA , Beijing, China
                [3] 3College of Food Science and Nutritional Engineering, China Agricultural University , Beijing, China
                Author notes

                Edited by: Ricardo Araujo, Universidade do Porto, Portugal

                Reviewed by: Gerard M. Moloney, University College Cork, Ireland; Aurelijus Burokas, Vilnius University, Lithuania; Silvia Leoncini, Azienda Ospedaliera Universitaria Senese, Italy

                *Correspondence: Yunsheng Yang, sunnyddc@ 123456plagh.org
                Article
                10.3389/fmicb.2023.1278162
                10704100
                38075901
                ad3d84d1-3e20-4794-9f76-e3c7a755a815
                Copyright © 2023 Li, Zhang, Luo, Meng, Zhong, Zheng and Yang.

                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
                : 15 August 2023
                : 16 October 2023
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 125, Pages: 19, Words: 15086
                Funding
                Funded by: Translational Medicine Project of Chinese PLA General Hospital
                Award ID: 2017TM-002
                The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.
                Categories
                Microbiology
                Original Research
                Custom metadata
                Microorganisms in Vertebrate Digestive Systems

                Microbiology & Virology
                apis mellifera,autism,human fecal microbiota,cognitive impairment,microbiota-gut-brain axis

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