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The Gill-Associated Symbiont Microbiome Is a Main Source of Woody-Plant

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The Gill-Associated Symbiont Microbiome Is a Main Source of Woody-Plant bioRxiv preprint doi: https://doi.org/10.1101/357616; this version posted June 27, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 The gill-associated symbiont microbiome is a main source of woody-plant 2 polysaccharide hydrolase genes and secondary metabolite gene clusters in 3 Neoteredo reynei, a unique shipworm from south Atlantic mangroves. 4 5 Thais L. Brito1, Amanda B. Campos2, F.A. Bastiaan von Meijenfeldt3, Julio P. Daniel1, Gabriella 6 B. Ribeiro1, Genivaldo G. Z. Silva4; Diego V. Wilke1; Daniela Morais5, Bas E. Dutilh3,6, Pedro M. 7 Meirelles2, Amaro E. Tridade-Silva1. 8 9 1 Drug Research and Development Center, Department of Physiology and Pharmacology, Federal 10 University of Ceara, Fortaleza, CE, Brazil; 11 2 Institute of Biology, Federal University of Bahia, Salvador, BA, Brazil 12 3 Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, Netherlands; 13 4 Computational Science Research Center, San Diego State University, San Diego, 14 CA, USA; 15 5 National Institute of Metrology, Quality and Technology, Rio de Janeiro, Brazil; 16 6 Centre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, 17 Nijmegen, The Netherlands. 18 19 * Corresponding author 20 E-mail: [email protected] (AETS) 21 22 23 1 bioRxiv preprint doi: https://doi.org/10.1101/357616; this version posted June 27, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 24 Abstract 25 26 Teredinidae is a family of highly adapted wood-feeding and wood-boring bivalves, 27 commonly known as shipworms, whose evolution is linked to the acquisition of cellulolytic 28 gammaproteobacterial symbionts harbored in bacteriocytes within the gills. In the present work 29 we applied metagenomics to characterize microbiomes of the gills and digestive tract of Neoteredo 30 reynei, a mangrove-adapted shipworm species found over a large range of the Brazilian coast. 31 Comparative metagenomics grouped the symbiotic gammaproteobacterial community of gills of 32 different N. reynei specimens, indicating closely related bacterial types are shared, while intestine 33 and digestive glands presented related, and more diverse microbiomes that did not overlap with 34 gills. Annotation of assembled metagenomic contigs revealed that the symbiotic community of N. 35 reynei gills was a hotspot of woody-polysaccharides degrading hydrolase genes, and Biosynthetic 36 Gene Clusters (BGCs), while in contrast, the digestive tract microbiomes seems to play little role 37 in wood digestion and secondary metabolites biosynthesis. Metagenome binning recovered the 38 nearly complete genome sequences of two symbiotic Teredinibacter strains from the gills, a 39 representative of Teredinibacter turnerae “clade I” strain, and a yet to be cultivated Teredinibacter 40 sp. type. These Teredinibacter genomes, as well as unbinned gill-derived gammaproteobacteria 41 contigs, code for novelty including an endo-β-1,4-xylanase/acetylxylan esterase multi-catalytic 42 carbohydrate-active enzyme, and a trans-acyltransferase polyketide synthase (trans-AT PKS) gene 43 cluster with the gene cassette for generating -branching on complex polyketides. Multivariate 44 analyzes have shown that the secondary metabolome encoded on the genomes of Teredinibacter 45 representatives, including the genomes binned from N. reynei gills’ metagenomes, stand out within 46 the Cellvibrionaceae family by size, and enrichments for polyketide, nonribosomal peptide and 2 bioRxiv preprint doi: https://doi.org/10.1101/357616; this version posted June 27, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 47 hybrid BGCs. Results grouped here add to the growing characterization of shipworm symbiotic 48 microbiomes and indicate that the N. reynei gill gammaproteobacterial community is a prolific 49 source of biotechnologically relevant enzymes for wood-digestion and bioactive compounds 50 production. 51 52 Introduction 53 54 Teredinidae, a family of obligate xylotrepetic (wood-boring) and xylotrophic (wood 55 feeding) mollusks, evolved from an ancestor lineage within the eulamellibranch order Myoida, 56 and succeeded in exploiting wood as new food source, most probably by concomitantly acquiring 57 cellulolytic bacterial symbionts [1]. These animals suffered dramatic body shape adaptations to 58 thrive as wood feeders including greatly reduced and burrowing-specialized valves (shells), and a 59 wood-sheltered worm-like body plan protruding from their shells, which led to their common name 60 of shipworms[2]. 61 Shipworm bacterial symbiotic communities are formed by cultivated and as yet 62 uncultivated closely related gammaproteobacteria, located intracellularly in bacteriocytes within 63 the gills (ctenidia) tissue [3–6]. The prototypical shipworm symbiont is the cellulolytic and 64 nitrogen fixing bacterium T. turnerae, isolated from a great variety of Teredinidae species from all 65 over the globe [7,8]. Sequencing of the complete genome of one strain of T. turnerae, T7901, 66 revealed that the genome of this bacterium codes for an arsenal of enzymes specialized in breaking 67 down woody material, reinforcing the hypothesis that shipworm gammaproteobacterial symbionts 68 play a critical role on supporting host nutrition[9]. Indeed, two seminal works provided strong 69 evidence for this hypothesis: firstly multi isotopic mass spectroscopy (MIMS) combined with 3 bioRxiv preprint doi: https://doi.org/10.1101/357616; this version posted June 27, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 70 transmission electron microscopy (TEM) showed, in Lyrodus pedicellatus, that T. turnerae cells 71 could fix atmospheric N2 in symbio, and then transfer nitrogenized compounds to their host [10]. 72 Secondly, a combination of metagenomics and proteomics of Bankia setacea, showed that wood- 73 specialized hydrolytic enzymes secreted by the symbiotic community are, somehow, selectively 74 conducted from the gill symbiotic site up to the host’s cecum to reach their substrates, the ingested 75 wood particles [11]. 76 Characterization of the T. turnerae T7901 genome also revealed that this endosymbiotic 77 bacterium contains a diversity of Biosynthetic Gene Clusters (BGCs) for secondary metabolites 78 comparable to those observed in free-living Streptomyces species known for their proficiency at 79 secondary metabolite production[9]. Indeed, compounds of the tartrolon family of boronated 80 antibiotic [12], and a novel triscatecholate siderophore called turnerbactin [13], were purified from 81 chemical extracts of T. turnerae cultures and had their respective biosynthetic routes identified 82 and characterized by retrobiosynthetic and phylogenetic approaches. Moreover, both BGCs were 83 proven to be expressed in symbio and signatures of these compounds were detected by mass 84 spectroscopy of shipworms whole animal extracts [12,13]. Such results fueled a hypothesis that 85 bioactive secondary metabolites could also play a role in supporting the symbiosis by providing 86 chemical defense and so, improving holobiont fitness [14], and/or mediate 87 competition/specialization to shape the distribution of bacterial types within the gills. Fluorescence 88 in situ hybridization (FISH) and confocal microscopy surveys of tissues from several shipworm 89 species provided evidence supporting both these hypothesis, showing that i) symbiotic 90 gammaproteobacterial types are structured within the gills, in separated niches of bacteriocytes, 91 and ii) tissues of the shipworm digestive system are virtually sterile (cecum) or containing a 92 discrete microbial community (intestine) [11,15]. 4 bioRxiv preprint doi: https://doi.org/10.1101/357616; this version posted June 27, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 93 Recently, the gill symbiotic community of the giant shipworm Kuphus polythalamia, a rare 94 species that burrows into mud and sediment instead of wood, was shown to be composed of sulfur 95 oxidizing chemoautotrophic gammaproteobacteria instead of Teredinibacter-related cellulolytic 96 types [16]. These findings suggested this bivalve is a chemoautotrophic descendent of a 97 xylotrophic ancestor, thus adding complexity to the biology of symbiosis in the family. N. reynei 98 is another singular shipworm that has been reported on mangroves of the south Atlantic, including 99 records of a large range of the 7.367 km long Brazilian coastline, from the States of Pará, at the 100 north of the country, to Santa Catarina, at the very south. N. reynei is the only species of the genus, 101 and can be rapidly identified by a unique feature: the presence of large
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