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Unraveling the Physiological Roles of the Cyanobacterium Geitlerinema Sp

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Unraveling the Physiological Roles of the Cyanobacterium Geitlerinema Sp RESEARCH ARTICLE Unraveling the Physiological Roles of the Cyanobacterium Geitlerinema sp. BBD and Other Black Band Disease Community Members through Genomic Analysis of a Mixed Culture Paul A. Den Uyl1, Laurie L. Richardson4, Sunit Jain1, Gregory J. Dick1,2,3* a11111 1 Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, 48109–1005, United States of America, 2 Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109–1048, United States of America, 3 Center for Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI, 48109–2218, United States of America, 4 Department of Biological Sciences, Florida International University, Miami, FL 33199, United States of America * [email protected] OPEN ACCESS Citation: Den Uyl PA, Richardson LL, Jain S, Dick GJ (2016) Unraveling the Physiological Roles of the Abstract Cyanobacterium Geitlerinema sp. BBD and Other Black Band Disease Community Members through Black band disease (BBD) is a cyanobacterial-dominated polymicrobial mat that propagates Genomic Analysis of a Mixed Culture. PLoS ONE 11 on and migrates across coral surfaces, necrotizing coral tissue. Culture-based laboratory (6): e0157953. doi:10.1371/journal.pone.0157953 studies have investigated cyanobacteria and heterotrophic bacteria isolated from BBD, but Editor: Christina A. Kellogg, U.S. Geological Survey, the metabolic potential of various BBD microbial community members and interactions UNITED STATES between them remain poorly understood. Here we report genomic insights into the physio- Received: April 19, 2016 logical and metabolic potential of the BBD-associated cyanobacterium Geitlerinema sp. Accepted: June 7, 2016 BBD 1991 and six associated bacteria that were also present in the non-axenic culture. The Published: June 23, 2016 essentially complete genome of Geitlerinema sp. BBD 1991 contains a sulfide quinone oxi- doreductase gene for oxidation of sulfide, suggesting a mechanism for tolerating the sulfidic Copyright: © 2016 Den Uyl et al. This is an open access article distributed under the terms of the conditions of BBD mats. Although the operon for biosynthesis of the cyanotoxin microcystin Creative Commons Attribution License, which permits was surprisingly absent, potential relics were identified. Genomic evidence for mixed-acid unrestricted use, distribution, and reproduction in any fermentation indicates a strategy for energy metabolism under the anaerobic conditions medium, provided the original author and source are credited. present in BBD during darkness. Fermentation products may supply carbon to BBD hetero- trophic bacteria. Among the six associated bacteria in the culture, two are closely related to Data Availability Statement: Contig sequences, bins, and annotations are publicly available on the organisms found in culture-independent studies of diseased corals. Their metabolic path- Integrated Microbial Genomes website under IMG ways for carbon and sulfur cycling, energy metabolism, and mechanisms for resisting coral Genome ID 3300001677 and in Genbank under defenses suggest adaptations to the coral surface environment and biogeochemical roles BioProject PRJNA281489, accession numbers within the BBD mat. Polysulfide reductases were identified in a Flammeovirgaceae genome LWRO00000000, LYSV00000000, LYSW00000000, LYSX00000000, LYSY00000000, LYSZ00000000, (Bacteroidetes) and the sox pathway for sulfur oxidation was found in the genome of a Rho- and LYTA00000000. dospirillales bacterium (Alphaproteobacteria), revealing mechanisms for sulfur cycling, Funding: This work was supported by National which influences virulence of BBD. Each genomic bin possessed a pathway for conserving Science Foundation (http://www.nsf.gov) grant energy from glycerol degradation, reflecting adaptations to the glycerol-rich coral environ- EAR1035955 and an Alfred P. Sloan Foundation ment. The presence of genes for detoxification of reactive oxygen species and resistance to (http://www.sloan.org) Fellowship (grant number PLOS ONE | DOI:10.1371/journal.pone.0157953 June 23, 2016 1/19 Genomic Analysis of Geitlerinema sp. BBD and Co-Cultured Bacteria BR2013-027) in Ocean Sciences to GJD and antibiotics suggest mechanisms for combating coral defense strategies. This study builds National Science Foundation (http://www.nsf.gov) upon previous research on BBD and provides new insights into BBD disease etiology. award OCE-1208784 to LLR. Competing Interests: The authors have declared that no competing interests exist. Introduction Coral reefs are a diverse and resource-rich habitat, teeming with biological activity that sup- ports an estimated 25% of all marine life. Yet it is well known that coral reefs are degrading on a worldwide basis. In particular, coral diseases, including black band disease (BBD), are recog- nized as a significant threat to coral reefs and associated ecosystem services [1, 2]. BBD is characterized by a dark cyanobacterial-dominated mat that is present as a band that migrates across the surface of infected corals [3]. It is similar to cyanobacterial mats found in other environments, such as hot spring outflows and hypersaline benthic zones, in that it con- tains strong vertical microgradients of oxygen and sulfide within the 1 mm thick band [4]. Studies using oxygen and sulfide sensitive microelectrodes have revealed that the band is fully anoxic and sulfide-rich at night, while during the day the surface of the band is supersaturated with oxygen. The oxygen/sulfide interface migrates vertically within the mat throughout the day/night cycle [4]. The band, which is dark red due to the cyanobacterial pigment phycoery- thrin and appears black in situ, is known to consist of a pathogenic, polymicrobial community that includes, in addition to photosynthetic cyanobacteria, large populations of sulfate reducing bacteria, sulfide oxidizing bacteria, and numerous bacterial heterotrophs [5, 6]. Physiological processes of these BBD community members create and maintain the dynamic BBD chemical microenvironment, which is an important factor in pathogenicity [6, 7, 8, 9]. As the band moves across a coral colony, typically at rates of approximately 3 mm/day, but up to 1 cm/ day, it completely lyses coral tissue, leaving behind exposed coral skeleton. Coral tissue lysis is the result of exposure to the band itself, which is anoxic at the base and contains at least two toxins, sulfide and microcystin. The combination of anoxia and these toxins has been experimentally shown to lyse living coral tissue [10, 11]. For many BBD-susceptible corals, particularly sclerac- tinian corals which grow on the order of 1 cm in circumference per year, the rate of tissue lysis can cause complete mortality of entire coral colonies and thus impact the biological and geo- logical structure of coral reef environments [12, 13]. The dominance of the BBD microbial mat by gliding, filamentous, non-heterocystous cya- nobacteria has been recognized since the first observations of BBD by Antonius in the 1970s [14, 15]. It is now known that, on a worldwide basis, there is one dominant BBD cyanobacterial ribotype, recently classified as the new genus and species Roseofilum reptotaenium [16, 17]. This ribotype has been found in BBD throughout the Caribbean [18], as well as on the Great Barrier Reef [19] and in the Red Sea [20]. Unlike BBD in the Indo-Pacific and the Red Sea, BBD in the Caribbean has been shown to contain several additional genera of cyanobacteria [21, 18], all of which have been shown to produce the cyanotoxin microcystin [22, 23, 24, 25]. In addition to toxin production, BBD cyanobacterial filaments play an important role in BBD by forming the physical matrix of the mat community [11]. The BBD microbial mat also contains a diversity of non-photosynthetic bacteria, some of which have been proposed as BBD pathogens [26]. These include sulfide-oxidizing bacteria, sulfate-reducing bacteria, and other heterotrophic bacteria [26, 27, 28, 29, 30]. The sulfide pro- duced in the mat has been attributed to dissimilatory sulfate-reducing bacteria, primarily of the genus Desulfovibrio [27, 31]. Sulfide-oxidizing bacteria associated with BBD include Beggiatoa [32] and others [33], and may potentially play a role in detoxification of sulfide. A wide variety PLOS ONE | DOI:10.1371/journal.pone.0157953 June 23, 2016 2/19 Genomic Analysis of Geitlerinema sp. BBD and Co-Cultured Bacteria of BBD heterotrophic bacteria have been detected in BBD, but little is known about them beyond their taxonomy. The composition of this community was recently characterized through a meta-analysis of 87 published 16S rRNA gene clone libraries produced from individ- ual samples of BBD [33]. Cyanobacteria are an important component of the pathogenesis of BBD. While some BBD cyanobacteria have been isolated into culture in the laboratory, none are axenic, and it may be that they require associated bacteria to thrive (discussed in [16]). However, laboratory experi- ments with non-axenic cultures have provided much useful information about the ecological physiology of BBD cyanobacteria and their relationship to BBD etiology. One such culture, desig- nated Geitlerinema BBD 1991, was derived from a single BBD cyanobacterial filament and con- sists of the cyanobacterium Geitlerinema sp. BBD 1991 and several other bacteria presumably sourced from BBD [34]. This mixed culture has been extensively studied, and has provided insights into BBD cyanobacterial primary and secondary metabolism as well as how these
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