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Prevalence,complete genome,and metabolic potentials of a phylogenetically novel cyanobacterial symbiont in the coral-killing sponge,Terpios hoshinota
Authors:Yu-Hsiang Chen  Hsing-Ju Chen  Cheng-Yu Yang  Jia-Ho Shiu  Daphne Z. Hoh  Pei-Wen Chiang  Wenhua Savanna Chow  Chaolun Allen Chen  Tin-Han Shih  Szu-Hsien Lin  Chi-Ming Yang  James Davis Reimer  Euichi Hirose  Budhi Hascaryo Iskandar  Hui Huang  Peter J. Schupp  Chun Hong James Tan  Hideyuki Yamashiro  Ming-Hui Liao  Sen-Lin Tang
Affiliation:1. Bioinformatics Program, Taiwan International Graduate Program, National Taiwan University, Taipei, Taiwan;2. Biodiversity Research Center, Academia Sinica, Taipei, Taiwan

These authors contributed equally to this work.;3. Biodiversity Research Center, Academia Sinica, Taipei, Taiwan;4. Biodiversity Research Center, Academia Sinica, Taipei, Taiwan

Biodiversity Program, Taiwan International Graduate Program, Academia Sinica and National Taiwan Normal University, Taipei, Taiwan

Department of Life Science, National Taiwan Normal University, Taipei, Taiwan;5. Biodiversity Research Center, Academia Sinica, Taipei, Taiwan

Biodiversity Program, Taiwan International Graduate Program, Academia Sinica and National Taiwan Normal University, Taipei, Taiwan;6. Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, Nishihara, Okinawa, Japan

Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, Japan;7. Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, Nishihara, Okinawa, Japan;8. Department of Fishery Resources Utilization, Faculty of Fisheries and Marine Science, Bogor Agricultural University, Bogor, Indonesia;9. Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya, China;10. Institute of Chemistry and Biology of the Marine Environment, University of Oldenburg, Wilhelmshaven, Germany;11. Faculty of Science and Marine Environment, Universiti Malaysia Terengganu, Kuala Nerus, Terengganu, Malaysia

Institute of Oceanography and Environment, Universiti Malaysia Terengganu, Kuala Nerus, Terengganu, Malaysia;12. Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, Japan;13. Bioinformatics Program, Institute of Information Science, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan

Abstract:Terpios hoshinota is an aggressive, space-competing sponge that kills various stony corals. Outbreaks of this species have led to intense damage to coral reefs in many locations. Here, the first large-scale 16S rRNA gene survey across three oceans revealed that bacteria related to the taxa Prochloron, Endozoicomonas, SAR116, Ruegeria, and unclassified Proteobacteria were prevalent in T. hoshinota. A Prochloron-related bacterium was the most dominant and prevalent cyanobacterium in T. hoshinota. The complete genome of this uncultivated cyanobacterium and pigment analysis demonstrated that it has phycobiliproteins and lacks chlorophyll b, which is inconsistent with the definition of Prochloron. Furthermore, the cyanobacterium was phylogenetically distinct from Prochloron, strongly suggesting that it should be a sister taxon to Prochloron. Therefore, we proposed this symbiotic cyanobacterium as a novel species under the new genus Candidatus Paraprochloron terpiosi. Comparative genomic analyses revealed that ‘Paraprochloron’ and Prochloron exhibit distinct genomic features and DNA replication machinery. We also characterized the metabolic potentials of ‘Paraprochloron terpiosi’ in carbon and nitrogen cycling and propose a model for interactions between it and T. hoshinota. This study builds a foundation for the study of the T. hoshinota microbiome and paves the way for better understanding of ecosystems involving this coral-killing sponge.
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