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      How Does Tremblaya princeps Get Essential Proteins from Its Nested Partner Moranella endobia in the Mealybug Planoccocus citri?

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          Many insects maintain intracellular mutualistic symbiosis with a wide range of bacteria which are considered essential for their survival (primary or P-endosymbiont) and typically suffer drastic genome degradation. Progressive loss of P-endosymbiont metabolic capabilities could lead to the recruitment of co-existent facultative endosymbiont (secondary or S-endosymbiont), thus adding more complexity to the symbiotic system. Planococcus citri, among other mealybug species, harbors an unconventional nested endosymbiotic system where every Tremblaya princeps cell (β-proteobacterium) harbors many Moranella endobia cells (γ-proteobacterium). In this system, T. princeps possess one of the smallest prokaryote genome known so far. This extreme genome reduction suggests the supply of many metabolites and essential gene products by M. endobia. Although sporadic cell lysis is plausible, the bacterial participation on the regulation of the predicted molecular exchange (at least to some extent) cannot be excluded. Although the comprehensive analysis of the protein translocation ability of M. endobia PCVAL rules out the existence of specific mechanisms for the exportation of proteins from M. endobia to T. princeps, immunolocation of two M. endobia proteins points towards a non-massive but controlled protein provision. We propose a sporadic pattern for the predicted protein exportation events, which could be putatively controlled by the host and/or mediated by local osmotic stress.

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          Most cited references 39

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          Clustal W and Clustal X version 2.0.

          The Clustal W and Clustal X multiple sequence alignment programs have been completely rewritten in C++. This will facilitate the further development of the alignment algorithms in the future and has allowed proper porting of the programs to the latest versions of Linux, Macintosh and Windows operating systems. The programs can be run on-line from the EBI web server: The source code and executables for Windows, Linux and Macintosh computers are available from the EBI ftp site
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            SignalP 4.0: discriminating signal peptides from transmembrane regions.

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              Extreme genome reduction in symbiotic bacteria.

              Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.

                Author and article information

                Role: Editor
                PLoS One
                PLoS ONE
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                21 October 2013
                : 8
                : 10
                [1 ]Institut Cavanilles de Biodiversitat y Biologia Evolutiva, Universitat de València, Paterna (València), Spain
                [2 ]UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, INSA-Lyon, INRA, Villeurbanne, France
                [3 ]Área de Genómica y Salud, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana FISABIO – Salud Pública, València, Spain
                University of South Florida College of Medicine, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: RG SLM AL AH AM. Performed the experiments: SLM SB. Analyzed the data: SLM RG AH. Contributed reagents/materials/analysis tools: AL AM AH RG SLM. Wrote the paper: SLM RG AL.


                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 7
                Financial support was provided by grants BFU2012-39816-C02-01 (Ministerio de Economía y Competitividad, Spain; to A. Latorre, Prometeo/2009/092 (Conselleria d’Educació, Generalitat Valenciana, Spain; to A. Moya, and ANR-2010-BLAN-170101 (ImmunSymbArt; to A. Heddi. S. López-Madrigal is a recipient of a fellowship from the Ministerio de Educación (Spain; The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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