School of BioSciences - Research Publications

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    Intracellular Bacterial Symbionts in Corals: Challenges and Future Directions
    Maire, J ; Blackall, LL ; van Oppen, MJH (MDPI, 2021-11)
    Corals are the main primary producers of coral reefs and build the three-dimensional reef structure that provides habitat to more than 25% of all marine eukaryotes. They harbor a complex consortium of microorganisms, including bacteria, archaea, fungi, viruses, and protists, which they rely on for their survival. The symbiosis between corals and bacteria is poorly studied, and their symbiotic relationships with intracellular bacteria are only just beginning to be acknowledged. In this review, we emphasize the importance of characterizing intracellular bacteria associated with corals and explore how successful approaches used to study such microorganisms in other systems could be adapted for research on corals. We propose a framework for the description, identification, and functional characterization of coral-associated intracellular bacterial symbionts. Finally, we highlight the possible value of intracellular bacteria in microbiome manipulation and mitigating coral bleaching.
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    The transposable element-rich genome of the cereal pest Sitophilus oryzae
    Parisot, N ; Vargas-Chavez, C ; Goubert, C ; Baa-Puyoulet, P ; Balmand, S ; Beranger, L ; Blanc, C ; Bonnamour, A ; Boulesteix, M ; Burlet, N ; Calevro, F ; Callaerts, P ; Chancy, T ; Charles, H ; Colella, S ; Barbosa, ADS ; Dell'Aglio, E ; Di Genova, A ; Febvay, G ; Gabaldon, T ; Ferrarini, MG ; Gerber, A ; Gillet, B ; Hubley, R ; Hughes, S ; Jacquin-Joly, E ; Maire, J ; Marcet-Houben, M ; Masson, F ; Meslin, C ; Montagne, N ; Moya, A ; Ribeiro de Vasconcelos, AT ; Richard, G ; Rosen, J ; Sagot, M-F ; Smit, AFA ; Storer, JM ; Vincent-Monegat, C ; Vallier, A ; Vigneron, A ; Zaidman-Remy, A ; Zamoum, W ; Vieira, C ; Rebollo, R ; Latorre, A ; Heddi, A (BMC, 2021-11-09)
    BACKGROUND: The rice weevil Sitophilus oryzae is one of the most important agricultural pests, causing extensive damage to cereal in fields and to stored grains. S. oryzae has an intracellular symbiotic relationship (endosymbiosis) with the Gram-negative bacterium Sodalis pierantonius and is a valuable model to decipher host-symbiont molecular interactions. RESULTS: We sequenced the Sitophilus oryzae genome using a combination of short and long reads to produce the best assembly for a Curculionidae species to date. We show that S. oryzae has undergone successive bursts of transposable element (TE) amplification, representing 72% of the genome. In addition, we show that many TE families are transcriptionally active, and changes in their expression are associated with insect endosymbiotic state. S. oryzae has undergone a high gene expansion rate, when compared to other beetles. Reconstruction of host-symbiont metabolic networks revealed that, despite its recent association with cereal weevils (30 kyear), S. pierantonius relies on the host for several amino acids and nucleotides to survive and to produce vitamins and essential amino acids required for insect development and cuticle biosynthesis. CONCLUSIONS: Here we present the genome of an agricultural pest beetle, which may act as a foundation for pest control. In addition, S. oryzae may be a useful model for endosymbiosis, and studying TE evolution and regulation, along with the impact of TEs on eukaryotic genomes.
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    Microbiome characterization of defensive tissues in the model anemone Exaiptasia diaphana
    Maire, J ; Blackall, LL ; van Oppen, MJH (BMC, 2021-05-21)
    BACKGROUND: Coral reefs are among the most diverse and productive ecosystems on Earth. This success relies on the coral's association with a wide range of microorganisms, including dinoflagellates of the family Symbiodiniaceae that provide coral hosts with most of their organic carbon requirements. While bacterial associates have long been overlooked, research on these microorganisms is gaining traction, and deciphering bacterial identity and function is greatly enhancing our understanding of cnidarian biology. Here, we investigated bacterial communities in defensive tissues (acontia) of the coral model, the sea anemone Exaiptasia diaphana. Acontia are internal filaments that are ejected upon detection of an external threat and release toxins to repel predators. RESULTS: Using culturing techniques and 16S rRNA gene metabarcoding we identified bacterial communities associated with acontia of four Great Barrier Reef-sourced E. diaphana genotypes. We show that bacterial communities are similar across genotypes, and dominated by Alteromonadaceae, Vibrionaceae, Rhodobacteraceae, and Saprospiraceae. By analyzing abundant amplicon sequence variants (ASVs) from metabarcoding data from acontia and comparing these to data from whole anemones, we identified five potentially important bacterial genera of the acontia microbiome: Vibrio, Sulfitobacter, Marivita, Alteromonas, and Lewinella. The role of these bacteria within the acontia remains uninvestigated but could entail assistance in defense processes such as toxin production. CONCLUSIONS: This study provides insight into potential bacterial involvement in cnidarian defense tissues and highlights the need to study bacterial communities in individual compartments within a holobiont.
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    Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs
    Maire, J ; Girvan, SK ; Barkla, SE ; Perez-Gonzalez, A ; Suggett, DJ ; Blackall, LL ; van Oppen, MJH (SPRINGERNATURE, 2021-07)
    Corals house a variety of microorganisms which they depend on for their survival, including endosymbiotic dinoflagellates (Symbiodiniaceae) and bacteria. While cnidarian-microorganism interactions are widely studied, Symbiodiniaceae-bacteria interactions are only just beginning to receive attention. Here, we describe the localization and composition of the bacterial communities associated with cultures of 11 Symbiodiniaceae strains from nine species and six genera. Three-dimensional confocal laser scanning and electron microscopy revealed bacteria are present inside the Symbiodiniaceae cells as well as closely associated with their external cell surface. Bacterial pure cultures and 16S rRNA gene metabarcoding from Symbiodiniaceae cultures highlighted distinct and highly diverse bacterial communities occur intracellularly, closely associated with the Symbiodiniaceae outer cell surface and loosely associated (i.e., in the surrounding culture media). The intracellular bacteria are highly conserved across Symbiodiniaceae species, suggesting they may be involved in Symbiodiniaceae physiology. Our findings provide unique new insights into the biology of Symbiodiniaceae.
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    Endosymbiosis morphological reorganization during metamorphosis diverges in weevils.
    Maire, J ; Chouaia, B ; Zaidman-Rémy, A ; Heddi, A (Informa UK Limited, 2020-11-02)
    Virtually all animals associate with beneficial symbiotic bacteria. Whether and how these associations are modulated across a host's lifecycle is an important question in disentangling animal-bacteria interactions. We recently reported a case of complete morphological reorganization of symbiosis during metamorphosis of the cereal weevil, Sitophilus oryzae. In this model, the bacteriome, a specialized organ that houses the intracellular bacterium Sodalis pierantonius, undergoes a two-phase remodeling program synchronously driven by host and endosymbiont, resulting in a localization shift and the formation of multiple new bacteriomes. Here, we provide comparative data in a closely-related coleopteran, the red palm weevil Rhynchophorus ferrugineus, which is associated with the ancestral endosymbiont Nardonella. Using cell imaging experiments, we show that the red pal weevil bacteriome remains unchanged during metamorphosis, hence contrasting with what we reported in the cereal weevil S. oryzae. These findings highlight the complexity and divergence of host-symbiont interactions and their intertwining with host development, even in closely-related species. Abbreviations: DAPI: 4',6-diamidino-2-phenylindole; FISH: Fluorescence in situ hybridization; T3SS: Type III secretion system.