Mussismilia braziliensis White Plague Disease Is Characterized by an Affected Coral Immune System and Dysbiosis

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Mussismilia braziliensis White Plague Disease Is Characterized by an Affected Coral Immune System and Dysbiosis A. W. Silva-Lima 1 & A. M. Froes 1 & G. D. Garcia 1,2 & L. A. C. Tonon 1,2 & J. Swings 1,2 & C. A. N. Cosenza 2 & M. Medina 3 & K. Penn 4 & J. R. Thompson 4 & C. C. Thompson 1,2 & F. L. Thompson 1,2 Received: 7 June 2019 / Accepted: 14 August 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Infectious diseases are one of the major drivers of coral reef decline worldwide. White plague-like disease (WPL) is a widespread disease with a complex etiology that infects several coral species, including the Brazilian endemic species Mussismilia braziliensis. Gene expression profiles of healthy and WPL-affected M. braziliensis were analyzed in winter and summer seasons. The de novo assembly of the M. braziliensis transcriptome from healthy and white plague samples produced a reference transcriptome containing 119,088 transcripts. WPL-diseased samples were characterized by repression of immune system and cellular defense processes. Autophagy and cellular adhesion transcripts were also repressed in WPL samples, suggesting exhaustion of the coral host defenses. Seasonal variation leads to plasticity in transcription with upregulation of intracellular signal transduction, apoptosis regulation, and oocyte development in the summer. Analysis of the active bacterial rRNA indicated that Pantoea bacteria were more abundant in WPL corals, while Tistlia, Fulvivirga, and Gammaproteobacteria Ga0077536 were more abundant in healthy samples. Cyanobacteria proliferation was also observed in WPL, mostly in the winter. These results indicate a scenario of dysbiosis in WPL-affected M. braziliensis, with the loss of potentially symbiotic bacteria and proliferation of opportunistic microbes after the start of the infection process. Keywords Coral reefs . Mussismilia braziliensis . White plague . Metatranscriptomic analysis . Dysbiosis

Introduction A worldwide decline in reef-building coral cover has been observed in recent decades due to a combination of local Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00248-020-01588-5) contains supplementary material, which is available to authorized users. * F. L. Thompson [email protected] 1

Laboratório de Microbiologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), Av. Carlos Chagas Fo. S/N-CCS-IB-Lab de Microbiologia-BLOCO A (Anexo) A3-sl 102, Cidade Universitária, Rio de Janeiro, RJ 21941-599, Brazil

2

Sage/Coppe, Centro de Gestão Tecnológica–CT2, Rua Moniz de Aragão, no. 360-Bloco 2, Ilha do Fundão-Cidade Universitária, Rio de Janeiro 21941-972, Brazil

3

Pennsylvania State University, 324 Mueller Lab, University Park, PA 16802, USA

4

Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA

and global changes [1]. Coral infectious diseases have also intensified, triggered by, for example, lo