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Microbiome of Trichodesmium Colonies from the North Pacific Subtropical Gyre

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Microbiome of Trichodesmium Colonies from the North Pacific Subtropical Gyre ORIGINAL RESEARCH published: 06 July 2017 doi: 10.3389/fmicb.2017.01122 Microbiome of Trichodesmium Colonies from the North Pacific Subtropical Gyre Mary R. Gradoville 1*†, Byron C. Crump 1, Ricardo M. Letelier 1, Matthew J. Church 2 and Angelicque E. White 1 1 College of Earth, Ocean and Atmospheric Sciences, Oregon State University, Corvallis, OR, United States, 2 Flathead Lake Biological Station, University of Montana, MT, United States Filamentous diazotrophic Cyanobacteria of the genus Trichodesmium, often found in colonial form, provide an important source of new nitrogen to tropical and subtropical marine ecosystems. Colonies are composed of several clades of Trichodesmium in association with a diverse community of bacterial and eukaryotic epibionts. We used high-throughput 16S rRNA and nifH gene sequencing, carbon (C) and dinitrogen (N2) fixation assays, and metagenomics to describe the diversity and functional potential of the microbiome associated with Trichodesmium colonies collected from the North Edited by: Sophie Rabouille, Pacific Subtropical Gyre (NPSG). The 16S rRNA and nifH gene sequences from Centre National de la Recherche hand-picked colonies were predominantly (>99%) from Trichodesmium Clade I (i.e., Scientifique (CNRS), France T. thiebautii), which is phylogenetically and ecologically distinct from the Clade III Reviewed by: Eric A. Webb, IMS101 isolate used in most laboratory studies. The bacterial epibiont communities University of Southern California, were dominated by Bacteroidetes, Alphaproteobacteria, and Gammaproteobacteria, United States including several taxa with a known preference for surface attachment, and were Alyson E. Santoro, University of California, Santa Barbara, relatively depleted in the unicellular Cyanobacteria and small photoheterotrophic United States bacteria that dominate NPSG surface waters. Sequencing the nifH gene (encoding a *Correspondence: subcomponent of the nitrogenase enzyme) identified non-Trichodesmium diazotrophs Mary R. Gradoville [email protected] that clustered predominantly among the Cluster III nifH sequence-types that includes †Present Address: putative anaerobic diazotrophs. Trichodesmium colonies may represent an important Mary R. Gradoville, habitat for these Cluster III diazotrophs, which were relatively rare in the surrounding Ocean Sciences Department, seawater. Sequence analyses of nifH gene transcripts revealed several cyanobacterial University of Santa Cruz, Santa Cruz, CA, United States groups, including heterocystous Richelia, associated with the colonies. Both the 16S rRNA and nifH datasets indicated strong differences between Trichodesmium Specialty section: epibionts and picoplankton in the surrounding seawater, and also between the epibionts This article was submitted to Aquatic Microbiology, inhabiting Trichodesmium puff and tuft colony morphologies. Metagenomic and 16S a section of the journal rRNA gene sequence analyses suggested that lineages typically associated with a Frontiers in Microbiology copiotrophic lifestyle comprised a large fraction of colony-associated epibionts, in Received: 29 December 2016 contrast to the streamlined genomes typical of bacterioplankton in these oligotrophic Accepted: 01 June 2017 Published: 06 July 2017 waters. Additionally, epibiont metagenomes were enriched in specific genes involved in Citation: phosphate and iron acquisition and denitrification pathways relative to surface seawater Gradoville MR, Crump BC, metagenomes. We propose that the unique microbial consortium inhabiting colonies has Letelier RM, Church MJ and White AE (2017) Microbiome of Trichodesmium a significant impact on the biogeochemical functioning of Trichodesmium colonies in Colonies from the North Pacific pelagic environments. Subtropical Gyre. Front. Microbiol. 8:1122. Keywords: Trichodesmium, marine microbiome, nifH diversity, heterotrophic marine diazotrophs, metagenomics, doi: 10.3389/fmicb.2017.01122 16S rRNA, nitrogen fixation Frontiers in Microbiology | www.frontiersin.org 1 July 2017 | Volume 8 | Article 1122 Gradoville et al. Microbiome of Trichodesmium Colonies INTRODUCTION N2. Phototrophs including filamentous Cyanobacteria (Siddiqui et al., 1992) and diatoms (Borstad and Borstad, 1977) have The filamentous, dinitrogen (N2)-fixing (diazotrophic) historically been observed within Trichodesmium colonies. More cyanobacterium Trichodesmium provides a major source recently, heterocystous cyanobacterial diazotrophs have been of bioavailable nitrogen (N) to the oligotrophic subtropical observed within Trichodesmium colonies (Momper et al., 2015) and tropical oceans (Karl et al., 2002; Capone et al., 2005). and nifH genes (encoding a subcomponent of the nitrogenase Trichodesmium abundances and N2 fixation rates have been enzyme) phylogenetically clustering among facultative anaerobes integral components of global N2 fixation estimates and models and aerobic heterotrophic bacteria have been retrieved from (e.g., Coles et al., 2004; Mahaffey et al., 2005); thus, an accurate Trichodesmium colonies (Gradoville et al., 2014). The degree to understanding of the physiology and ecology of this genus is which these associated diazotrophs contribute to bulk colony N2 crucial. Most Trichodesmium laboratory studies have used a fixation rates is unknown. single isolate, T. erythraeum strain IMS101, grown in culture Here, we examine the microbiome associated with with minimal heterotrophic bacteria. In contrast, natural Trichodesmium colonies collected from the North Pacific Trichodesmium populations are composed of species from four Subtropical Gyre (NPSG). We used a combined approach known phylogenetically distinct clades (Hynes et al., 2012), of high-throughput 16S rRNA and nifH gene sequencing, 13 15 which can vary in physiological traits, such as carbon (C) affinity metagenomics, and C and N2 fixation assays to survey and phosphonate biosynthesis (Dyhrman et al., 2009; Hutchins the diversity of the Trichodesmium holobiont, test for the et al., 2013). Furthermore, in nature they are commonly found presence and activity of non-Trichodesmium colony-associated associated with attached microorganisms (Borstad and Borstad, diazotrophs, and explore the functional potential of the 1977). The diversity of this complex community likely affects colonies. We compare the colony-associated microbiome the overall functioning of colonies (Gradoville et al., 2014), yet to the microbial community structure and metagenomic few studies have examined the ecology of Trichodesmium species composition of surrounding seawater, revealing diverse and and associated epibionts (although see Hmelo et al., 2012; Rouco unique microbial structure and functional potential associated et al., 2016). with Trichodesmium colonies. Trichodesmium cells exist as free filaments or aggregate colonies (Letelier and Karl, 1996) with varying morphologies, METHODS namely spherical “puffs” and fusiform “tufts.” These colonies have been reported to maintain an active and diverse Sample Collection assemblage of attached organisms, including bacteria, eukaryotic Samples were collected in March 2014 aboard the R/V Kilo phytoplankton, protozoa, fungi, and copepods (Borstad and Moana at Stn. ALOHA (A Long-term Oligotrophic Habitat Borstad, 1977; Sheridan et al., 2002). Trichodesmium colonies Assessment; 22.45◦N, 158◦W), an open-ocean field site ∼100 constitute a favorable environment for associated epibionts by km north of Oahu (Table 1). Trichodesmium colonies were providing buoyancy (Walsby, 1992), elevated concentrations of collected using a 202 µm plankton net which was hand- dissolved organic N (Capone et al., 1994), and a substrate for towed at <2kmh−1 through near-surface waters (<10 m depth) attachment (O’Neil, 1998). Recent studies using 16S rRNA gene for 10–15 min. Once recovered, colonies were isolated using sequencing have shown that Trichodesmium-associated bacterial an inoculating loop and rinsed twice with 0.2 µm-filtered epibionts include surface-associated taxa (Hmelo et al., 2012) surface seawater prior to all analyses. Colonies were sorted into and that selective processes appear to drive epibiont community morphological classes of spherical “puffs” (further divided into structure (Rouco et al., 2016). “radial puffs” and “non-radial puffs” on 23 Mar), fusiform “tufts,” Less is known about how associated microorganisms affect and “mixed” morphologies (Figure 1), and either filtered for the functioning of the Trichodesmium holobiont. Trichodesmium subsequent extraction of DNA and RNA or used for C and colonies appear to be hotspots for microbial activity: hydrolytic N2 fixation measurements. Additionally, bulk seawater from enzyme activities are elevated within colonies (Stihl et al., 25 m depth was collected for comparison with Trichodesmium 2001; Sheridan et al., 2002) and a metatranscriptome from colony DNA. Seawater samples were collected using sampling Trichodesmium bloom material recovered more transcripts from bottles attached to a CTD (conductivity, temperature, depth) associated organisms than from Trichodesmium cells (Hewson rosette, and subsampled into 4 L acid-washed, MilliQ-rinsed et al., 2009). Microbial processes carried out by associated polycarbonate bottles prior to filtration. microorganisms have the potential to influence rates of N2 or C fixation. For instance, quorum sensing by associated bacteria Carbon and Nitrogen Fixation Rates can increase alkaline phosphatase activity within colonies (Van Carbon (C) and dinitrogen (N2) fixation rates were measured Mooy et al., 2011), which could
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