Jellyfish Life Stages Shape Associated Microbial Communities

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Jellyfish Life Stages Shape Associated Microbial Communities fmicb-09-01534 July 10, 2018 Time: 16:16 # 1 ORIGINAL RESEARCH published: 12 July 2018 doi: 10.3389/fmicb.2018.01534 Jellyfish Life Stages Shape Associated Microbial Communities, While a Core Microbiome Is Maintained Across All Michael D. Lee1, Joshua D. Kling1, Rubén Araya2 and Janja Ceh2,3,4* 1 Department of Biological Sciences, University of Southern California, Los Angeles, CA, United States, 2 Instituto de Ciencias Naturales Alexander von Humboldt, Universidad de Antofagasta, Antofagasta, Chile, 3 Laboratory of Microbial Complexity and Functional Ecology, Institute of Antofagasta, University of Antofagasta, Antofagasta, Chile, 4 Centre for Biotechnology and Bioengineering, Universidad de Chile, Santiago, Chile The key to 650 million years of evolutionary success in jellyfish is adaptability: with alternating benthic and pelagic generations, sexual and asexual reproductive modes, multitudes of body forms and a cosmopolitan distribution, jellyfish are likely to have established a plenitude of microbial associations. Here we explored bacterial Edited by: assemblages in the scyphozoan jellyfish Chrysaora plocamia (Lesson 1832). Life stages Russell T. Hill, involved in propagation through cyst formation, i.e., the mother polyp, its dormant cysts University of Maryland Center for Environmental Science, (podocysts), and polyps recently excysted (excysts) from podocysts – were investigated. United States Associated bacterial assemblages were assessed using MiSeq Illumina paired-end tag Reviewed by: sequencing of the V1V2 region of the 16S rRNA gene. A microbial core-community was Detmer Sipkema, Wageningen University & Research, identified as present through all investigated life stages, including bacteria with closest Netherlands relatives known to be key drivers of carbon, nitrogen, phosphorus, and sulfur cycling. Jean-Christophe Auguet, Moreover, the fact that half of C. plocamia’s core bacteria were also present in life stages Centre National de la Recherche Scientifique (CNRS), France of the jellyfish Aurelia aurita, suggests that this bacterial community might represent an *Correspondence: intrinsic characteristic of scyphozoan jellyfish, contributing to their evolutionary success. Janja Ceh [email protected] Keywords: jellyfish microbiome, Chrysaora plocamia, jellyfish-bacteria, polyp stages, Humboldt Current System Specialty section: This article was submitted to INTRODUCTION Microbial Symbioses, a section of the journal Animals are becoming increasingly appreciated and studied as metaorganisms, or supraorganismal Frontiers in Microbiology structures, closely associated with multi-lineage consortia of microorganisms (i.e., bacteria, Received: 14 March 2018 archaea, eukaryotes, and viruses), together representing a dynamic assemblage that results in a co- Accepted: 20 June 2018 metabolism between the animal and its microbiome (McFall-Ngai et al., 2013). These relationships Published: 12 July 2018 have evolved so closely that in some cases host development depends on signals from these Citation: microbes, and its immune system may even recognize specific microbes as part of itself (Gilbert Lee MD, Kling JD, Araya R and Ceh J et al., 2012; McFall-Ngai et al., 2013). As bacterial life had already existed for about three billion (2018) Jellyfish Life Stages Shape years when animals first evolved (Knoll, 2015), microbe-animal interactions are likely as old as Associated Microbial Communities, animals themselves (Bosch, 2013). Based on their early appearance on the evolutionary scene, While a Core Microbiome Is Maintained Across All. cnidarians were likely amongst the first animals to establish associations with microorganisms. Front. Microbiol. 9:1534. With the four groups Anthozoa, Cubozoa, Hydrozoa, and Scyphozoa, the phylum is comprised doi: 10.3389/fmicb.2018.01534 of diverse taxa that inhabit all parts of the world’s ocean. A simple anatomy made up of two Frontiers in Microbiology| www.frontiersin.org 1 July 2018| Volume 9| Article 1534 fmicb-09-01534 July 10, 2018 Time: 16:16 # 2 Lee et al. Jellyfish Associated Bacteria germ layers, separated by an extracellular matrix, and highly ecosystems, and environmental conditions), jellyfish could complex stinging cells (cnidocytes) characterizes these basal be expected to benefit from a versatile microbiome that animals (Daly et al., 2007; Fautin, 2009; Rogers, 2009). may change in accordance with the current needs of the Within the cnidarians, corals and scyphozoans stand out as animal – or perhaps more aptly considered as a change in particularly important taxa: reef-building corals are important accordance with the current needs of the supraorganismal ecosystem engineers of high ecological and economic value, while structure. scyphozoans are infamous for their negative effect on marine The large and abundant jellyfish Chrysaora plocamia (Lesson ecosystems, fisheries and industries (Richardson et al., 2009; 1832) occurs along the Atlantic coast of South America, as well Graham et al., 2014). as in the Chilean-Peruvian Humboldt Current System where it A staggering level of developmental plasticity (Ceh et al., has been reported for its negative effects on anchovy fisheries 2015) and the ability to respond to spatiotemporal environmental and tourism (Quiñones et al., 2013). Its potential to severely alter fluctuations quickly allows scyphozoans to exploit a vast variety the highly productive Humboldt Current System (Thiel et al., of habitats and resources (Thein et al., 2013). Sexual reproduction 2007) makes it a key species to study (Riascos et al., 2013; Riascos in pelagic medusae results in a motile planula that settles in the et al., 2015). As in other Chrysaora species, e.g. in Chrysaora benthos, metamorphosizes, and grows into a polyp. Such polyps pacifica (Thein et al., 2013), cyst formation is the only known reproduce asexually, multiplying in numbers and producing mode for polyp propagation in C. plocamia, and therefore bears new medusae when environmental factors are appropriate. a particularly important role for the proliferation and survival of While most jellyfish-bloom studies have focused on the more this large and abundant jellyfish. conspicuous medusae, which appear seasonally in ocean surface Here, in an attempt to shed more light on bacteria associated waters, little is known about their polyp counterparts. However, with jellyfish, and how such associations may be involved in the relative longevity coupled with the potential to multiply in large important process of polyp proliferation via cyst formation, we numbers, and their capacity to withstand a wide range of adverse assessed microbial communities harbored by three life stages – environmental conditions, make the polyp a vital part of the polyps, podocysts, and excysts – in the jellyfish C. plocamia using scyphozoan life cycle. In fact, the capacity of scyphozoans to MiSeq Illumina paired-end tag sequencing of the V1V2 region of proliferate has been argued to reside in the sessile polyps (Arai, the 16S rRNA gene. 2009). Depending on the species, polyps can proliferate asexually in various ways (reviewed in Adler and Jarms, 2009), including MATERIALS AND METHODS cyst formation (Vagelli, 2007; Lucas et al., 2012), where polyps in the orders Rhizostomae (suborder Dactyliophorae) and Organism Collection and Maintenance Semaeostomae (Arai, 2009) form cysts against substrates by Polyp cultures were established from C. plocamia medusae pedal disks or stolons. These so called podocysts are chitin- collected at different times and in different places in Northern enclosed, contain stored reserves of organic compounds (Arai, Chile: in December 2014 and January 2015 in Bolsico 2009), and can stay dormant for long periods of time (Black, (23◦2700180S, 70◦3600080W); in February 2015 in Bahia Inglesa 1981; Thein et al., 2012). When appropriate environmental (27◦0600440S, 70◦5400520W); and in April 2015 in Mejillones conditions occur, a small polyp excysts and develops into a Bay (23◦0400230S, 70◦2400500W). Medusae were collected by fully functional polyp, capable of producing more podocysts scuba divers from a maximum depth of 15 m, caught with and medusae (Arai, 2009). The strategy of cyst formation a dip-net, individually placed into plastic bags, stored in a can contribute to an increase in polyp numbers, as well cooler, and transported to the laboratory for further processing. as to the animal’s survival, since podocysts are resilient to Oral arms were inspected for planulae, sectioned, and placed environmental conditions that polyps do not survive, e.g., onto a mesh (1 mm mesh-size) in a 10 L plastic box in severe hypoxia (Ishii et al., 2008; Levin et al., 2009; Thein 1 mm filtered seawater. To initiate shedding of planulae the et al., 2012) or predation by nudibranchs (Cargo and Schultz, container was slowly moved and the accumulated planulae were 1967). harvested from the bottom (Riascos et al., 2013; Ceh and Riascos, Being amongst the first and simplest animals existing, 2017). Two hundred planulae from individual medusae were cnidarians are an important group to investigate regarding the placed into individual plastic receptacles, containing 250 mL evolution of animal-microbial symbioses, and while bacterial of 1 mm filtered seawater and a settlement structure, i.e., a partners have been well studied in other cnidarians (Rosenberg plastic petri dish, placed upside-down on the water surface et al., 2007), investigating jellyfish-microbial interactions has for planulae to settle on the underside. Once most planulae only begun more recently
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