Microbial Processing of Jellyfish Detritus in the Ocean
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fmicb-11-590995 October 20, 2020 Time: 18:13 # 1 ORIGINAL RESEARCH published: 30 October 2020 doi: 10.3389/fmicb.2020.590995 Microbial Processing of Jellyfish Detritus in the Ocean Tinkara Tinta1,2*, Zihao Zhao1,3, Alvaro Escobar1, Katja Klun2, Barbara Bayer1†, Chie Amano1, Luca Bamonti1 and Gerhard J. Herndl1,3,4* 1 Department of Functional and Evolutionary Ecology, Bio-Oceanography Unit, Faculty of Life Sciences, University of Vienna, Vienna, Austria, 2 Marine Biology Station Piran, National Institute of Biology, Piran, Slovenia, 3 Vienna Metabolomics Center, University of Vienna, Vienna, Austria, 4 Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research (NIOZ), Utrecht University, Den Burg, Netherlands When jellyfish blooms decay, sinking jellyfish detrital organic matter (jelly-OM), rich in Edited by: proteins and characterized by a low C:N ratio, becomes a significant source of OM Youhei Yamashita, Hokkaido University, Japan for marine microorganisms. Yet, the key players and the process of microbial jelly- Reviewed by: OM degradation and the consequences for marine ecosystems remain unclear. We Yuya Tada, simulated the scenario potentially experienced by the coastal pelagic microbiome after National Institute for Minamata Disease, Japan the decay of a bloom of the cosmopolitan Aurelia aurita s.l. We show that about half Qi-Long Qin, of the jelly-OM is instantly available as dissolved organic matter and thus, exclusively Shandong University, China and readily accessible to microbes. During a typical decay of an A. aurita bloom in *Correspondence: the northern Adriatic Sea about 100 mg of jelly-OM L−1 becomes available, about Tinkara Tinta −1 −1 [email protected] 44 mmol L as dissolved organic carbon (DOC), 13 mmol L as total dissolved Gerhard J. Herndl nitrogen, 11 mmol L−1 of total hydrolyzable dissolved amino acids (THDAA) and [email protected] −1 3− 0.6 mmol L PO4 . The labile jelly-OM was degraded within 1.5 days (>98% of †Present address: Barbara Bayer, proteins, ∼70% of THDAA, 97% of dissolved free amino acids and the entire jelly- Department of Ecology, Evolution and DOC pool) by a consortium of Pseudoalteromonas, Alteromonas, and Vibrio. These Marine Biology, University of bacteria accounted for 90% of all metabolically active jelly-OM degraders, exhibiting California, Santa Barbara, Santa > Barbara, CA, United States high bacterial growth efficiencies. This implies that a major fraction of the detrital jelly- OM is rapidly incorporated into biomass by opportunistic bacteria. Microbial processing Specialty section: This article was submitted to of jelly-OM resulted in the accumulation of tryptophan, dissolved combined amino acids Aquatic Microbiology, and inorganic nutrients, with possible implications for biogeochemical cycles. a section of the journal Frontiers in Microbiology Keywords: jellyfish blooms, detritus, dissolved organic matter, marine microbial community, biodegradation, proteomics, biogeochemical cycles Received: 03 August 2020 Accepted: 30 September 2020 Published: 30 October 2020 INTRODUCTION Citation: Tinta T, Zhao Z, Escobar A, The complex pool of dissolved organic matter (DOM) in the oceans is one of the largest global Klun K, Bayer B, Amano C, Bamonti L reservoirs of carbon in the biosphere (662 Pg, Hansell et al., 2009). This DOM pool is almost and Herndl GJ (2020) Microbial Processing of Jellyfish Detritus exclusively accessible to diverse members of the microbial community affecting the biogeochemical in the Ocean. state of the ocean and thus the global climate (Azam and Malfatti, 2007). To predict the response of Front. Microbiol. 11:590995. marine ecosystems to natural and anthropogenic perturbations, our understanding on the relation doi: 10.3389/fmicb.2020.590995 between the organic matter (OM) field and the microbial consortia needs to be refined. Frontiers in Microbiology| www.frontiersin.org 1 October 2020| Volume 11| Article 590995 fmicb-11-590995 October 20, 2020 Time: 18:13 # 2 Tinta et al. Microbial Processing of Jellyfish Detritus One significant source of OM in the ocean that has been fragmented by predators and scavengers (Hays et al., 2018), so far largely overlooked are jellyfish (phylum Cnidaria, Class degraded by pelagic microbial communities (Titelman et al., Scyphozoa), which presumably account for >90% of the total 2006; Tinta et al., 2016) and/or massively deposited at the global gelatinous zooplankton biomass, estimated to represent seafloor (Lebrato et al., 2012), where they can be rapidly degraded 0.038 Pg C in the upper 200 m of the ocean (Lucas et al., by benthic communities (West et al., 2009; Sweetman et al., 2014). However, due to sampling biases and lack of data, 2016). Recent estimates on the transfer efficiency of jellyfish the global jellyfish biomass could be largely underestimated biomass indicate that jellyfish are an important component of the (Lebrato et al., 2019). In fact, jellyfish are ubiquitous and biological soft-tissue pump, potentially playing an important role important players in different ecosystems. When conditions as a food source for the food web of the ocean’s interior (Lebrato are favorable some jellyfish species form extensive blooms, et al., 2019). It has been demonstrated that jellyfish carcasses reaching high biomass within a short period of time by efficiently with their proteinaceous character, low C:N ratio and no hard grazing on phytoplankton, zooplankton and fish larvae (Acuña exoskeleton represent a high-quality substrate for specific pelagic et al., 2011; Pitt et al., 2013). Jellyfish blooms are often short- bacteria, altering diversity and functioning of marine food web lived and collapse abruptly due to various largely unexplored (Titelman et al., 2006; Tinta et al., 2012; Blanchet et al., 2015). C 3− environmental factors (Pitt et al., 2014; Schnedler-Meyer et al., Substantial accumulation of NH4 and PO4 has been recorded 2018; Goldstein and Steiner, 2020). Thus, with their “boom and as a result of microbial degradation of jelly-OM in the water bust” population dynamics, jellyfish can represent an important column (Tinta et al., 2010; Blanchet et al., 2015). Altogether, this perturbation to the surrounding ecosystem. Despite of the debate indicates that the pelagic microbial degradation of jelly-OM can over the reported global increase of their blooms and on the be rapid, with important implications for the fate of jelly-OM and actual cause of the observed jellyfish fluctuations, the increase biogeochemical cycles in the ocean. However, the key players and in their population size can have serious socio-economic and the rate and mechanisms of the microbial degradation process of ecological consequences (Richardson et al., 2009; Condon et al., pelagic jelly-OM remain unknown. 2012; Purcell, 2012; Sanz-Martín et al., 2016). It is undisputed, Here, we provide a detailed characterization of detrital however, that jellyfish represent a significant source of OM, jelly-OM and further insights into the processing of jelly-OM especially in coastal ecosystems where large blooms are regularly by microbial communities. To fully understand the nature reported (Kogovšek et al., 2010; Lucas et al., 2014). of the microbial interactions with jelly-OM we have scaled Yet, the link between jellyfish-derived OM and its our investigations down to the molecular level, i.e., the scale most probable consumers and degraders, i.e., the marine relevant for microbially mediated biochemical reactions (Azam microorganisms, has been addressed only by a few studies and Malfatti, 2007). We have characterized the detrital OM of (Titelman et al., 2006; Condon et al., 2011; Blanchet et al., 2015). the cosmopolitan coastal meroplanktonic scyphozoan Aurelia Alive jellyfish release copious amounts of colloidal and labile aurita s.l. on the individual compound level. We link the C-rich DOM via different mechanisms (i.e., sloppy feeding, remineralization rates of different jelly-OM compounds to the fecal pellets and mucus production, and excretion) (Condon metabolic activities of key microbial populations involved in the et al., 2010, 2011). It has been demonstrated that DOM released process. With this approach we ultimately tested the hypothesis by living jellyfish is rapidly respired rather than fueled into that jelly-OM is rapidly degraded by a small, but highly active the biomass production by otherwise rare members of the fraction of the pelagic microbial community. ambient microbial community (Condon et al., 2011; Dinasquet et al., 2013; Manzari et al., 2015). However, the significant fraction of the pelagic biomass that jellyfish incorporate during their life span becomes only available to consumers when MATERIALS AND METHODS jellyfish die. Some studies proposed that the OM release after a massive jellyfish die-off should be even higher and of different Sampling and Pre-processing of Jellyfish stoichiometry than the release from living jellyfish (Pitt et al., Biomass 2009). Jellyfish consist to >95% of water and the organic content Specimens of A. aurita s.l. were collected in the Gulf of Trieste, represents between 20 and 40% of their dry weight (Larson, northern Adriatic, during the senescent phase of their spring 1986; Lucas et al., 2011; Kogovšek et al., 2014), mainly in the 2018 bloom. Altogether, 27 moribund jellyfish specimens were form of proteins (Pitt et al., 2009). This is also reflected by the collected on different days (Supplementary Table S1). The low molar ratio of carbon to nitrogen (C:N = 4.5:1) of jellyfish conditions of the collected jellyfish specimens were evaluated biomass (Kogovšek et al., 2014; Molina-Ramírez et al., 2014). based on their activity (i.e., individuals had reduced bell pulsation Only recently, transcriptome profiling of some jellyfish species rate) and on the stage of their body deformation (i.e., individuals provided the baseline allowing first insights into the complexity had deformed bodies including reduced and/or absent oral arms). of this OM pool (Brekhman et al., 2015). Yet, the release rates Jellyfish were sampled individually from the surface of the water and the detailed biochemical composition of the OM of different column together with ambient seawater using a large acid- jellyfish taxa remain unknown.