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Bacterial Community Composition in the Sea Surface Microlayer Off the Peruvian Coast

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Bacterial Community Composition in the Sea Surface Microlayer Off the Peruvian Coast fmicb-09-02699 November 15, 2018 Time: 13:25 # 1 ORIGINAL RESEARCH published: 15 November 2018 doi: 10.3389/fmicb.2018.02699 Bacterial Community Composition in the Sea Surface Microlayer Off the Peruvian Coast Birthe Zäncker1*, Michael Cunliffe2,3 and Anja Engel1 1 GEOMAR – Helmholtz Centre for Ocean Research Kiel, Kiel, Germany, 2 Marine Biological Association of the United Kingdom, Plymouth, United Kingdom, 3 Marine Biology and Ecology Research Centre, School of Biological and Marine Sciences, Plymouth University, Plymouth, United Kingdom The sea surface microlayer (SML) is located at the air-sea interface, with microorganisms and organic matter in the SML influencing air-sea exchange processes. Yet understanding of the SML bacterial (bacterioneuston) community composition and assembly remains limited. Availability of organic matter, UV radiation and wind speed have previously been suggested to influence the community composition of Edited by: bacterioneuston. Another mechanism potentially controlling bacterioneuston dynamics Alison Buchan, is bacterioplankton attached to gel-like particles that ascend through the water University of Tennessee, Knoxville, United States column into the SML. We analyzed the bacterial community composition, Transparent Reviewed by: Exopolymer Particles (TEP) abundance and nutrient concentrations in the surface Zhanfei Liu, waters of the Peruvian upwelling region. The bacterioneuston and bacterioplankton University of Texas at Austin, United States communities were similar, suggesting a close spatial coupling. Four Bacteroidetes Xiao-Hua Zhang, families were significantly enriched in the SML, two of them, the Flavobacteriaceae and Ocean University of China, China Cryomorphaceae, were found to comprise the majority of SML-enriched operational *Correspondence: taxonomic units (OTUs). The enrichment of these families was controlled by a variety of Birthe Zäncker [email protected] environmental factors. The SML-enriched bacterial families were negatively correlated with water temperature and wind speed in the SML and positively correlated with Specialty section: nutrient concentrations, salinity and TEP in the underlying water (ULW). The correlations This article was submitted to Aquatic Microbiology, with nutrient concentrations and salinity suggest that the enriched bacterial families were a section of the journal more abundant at the upwelling stations. Frontiers in Microbiology Received: 23 July 2018 Keywords: microbial ecology, sea surface microlayer, SML, bacteria, cruise SO243, RV Sonne, peruvian upwelling Accepted: 23 October 2018 region, transparent exopolymer particles Published: 15 November 2018 Citation: INTRODUCTION Zäncker B, Cunliffe M and Engel A (2018) Bacterial Community Composition in the Sea Surface The sea surface microlayer (SML) constitutes the uppermost layer of the ocean, only 1– Microlayer Off the Peruvian Coast. 1000 mm thick, with unique chemical and biological properties that distinguish it from the Front. Microbiol. 9:2699. underlying water (ULW) (Zhang et al., 2003; Liss and Duce, 2005). Due to the location doi: 10.3389/fmicb.2018.02699 at the air-sea interface, the SML can influence exchange processes across this boundary Frontiers in Microbiology| www.frontiersin.org 1 November 2018| Volume 9| Article 2699 fmicb-09-02699 November 15, 2018 Time: 13:25 # 2 Zäncker et al. Bacteria in the Peruvian SML layer, such as air-sea gas exchange and the formation of sea spray attach to TEP in the water column (Schuster and Herndl, aerosols (Liss and Duce, 2005; Wurl and Holmes, 2008; Aller 1995; Mari and Kiorboe, 1996; Busch et al., 2017). TEP can et al., 2017; Engel et al., 2017). serve as microbial hotspots and can be used directly as a The term ‘neuston’ describes the organisms in the SML and substrate for bacterial degradation (Passow, 2002; Meiners et al., was first suggested by Naumann(1917). As in other marine 2008; Taylor and Cunliffe, 2017), and as grazing protection for ecosystems, bacterioneuston communities have important roles attached bacteria, e.g., by acting as an alternate food source for in SML functioning (Cunliffe et al., 2011). Bacterioneuston zooplankton (Malej and Harris, 1993; Passow and Alldredge, community composition of the SML has been analyzed and 1999; Dutz et al., 2005). TEP have also been suggested to serve as compared to the underlying water in different habitats with light protection for microorganisms in environments with high varying results, and has primarily focused on coastal waters irradiation (Ortega-Retuerta et al., 2009). and shelf seas, with limited study of the open ocean (Agogué This study focuses on understanding the bacterioneuston et al., 2005a; Franklin et al., 2005; Cunliffe et al., 2009c). In community composition as well as possible community control the North Sea, a distinct bacterial community was found in the mechanisms. Therefore, we analyzed the composition of the SML with Vibrio spp. and Pseudoalteromonas spp. dominating bacterial community in the SML and ULW as well as various the bacterioneuston (Franklin et al., 2005). During an artificially abiotic factors in addition to nutrients and TEP concentrations induced phytoplankton bloom in a fjord mesocosm experiment, during a cruise in the Peruvian upwelling region. the most dominant denaturing gradient gel electrophoresis (DGGE) bands of the bacterioneuston consisted of two bacterial families: Flavobacteriaceae and Alteromonadaceae (Cunliffe et al., MATERIALS AND METHODS 2009c). Other studies have however, found little or no differences in the bacterial community composition of the SML and the Sampling ULW (Agogué et al., 2005a; Obernosterer et al., 2008). Difficulties Samples were collected during the SO243 cruise to the Peruvian in direct comparisons between studies can arise because of the upwelling region onboard the RV Sonne from the 4th to the 22nd different methods used to sample the SML, which result in varied of October 2015 (Figure 1A), with 11 stations sampled between ◦ ◦ ◦ ◦ sampling depths (Agogué et al., 2004; Cunliffe et al., 2009a, 0 S and 15.7 S as well as 85.5 W and 75.3 W(Figure 1B). At 2011). each station, samples were collected from two depths: surface Even less is known about the community control mechanisms microlayer (SML) and underlying water (ULW) at 20 cm, except in the SML and how the bacterial community assembles at the air- at station 1 where an ULW sample was taken at 10 cm. SML sea interface. The bacterioneuston community could be altered sampling was conducted using a glass plate sampler from a zodiac by differing wind conditions and radiation levels (Agogué et al., (Harvey, 1966; Cunliffe and Wurl, 2014). The 50 × 26 cm silicate 2005b; Joux et al., 2006; Stolle et al., 2011; Rahlff et al., 2017), glass plate had an effective sampling surface area of 2600 cm2 with high wind speeds inhibiting the formation of a distinct considering both sides. For sampling, the zodiac was located app. bacterioneuston community (Stolle et al., 2011; Rahlff et al., 0.5 nautical miles into the wind direction away from the research 2017). Wind speed and radiation levels refer to external controls, vessel to avoid contamination. The glass plate was immersed however, bacterioneuston community composition might also be perpendicular to the sea surface and withdrawn at a controlled − influenced by internal factors such as nutrient availability and rate of ∼17 cm s 1. SML samples adhered to the plate and were organic matter (OM) produced either in the SML or in the ULW collected in an acid cleaned and rinsed bottle using a Teflon wiper (Azam et al., 1993; Judd et al., 2006; Nakajima et al., 2013). (Cunliffe and Wurl, 2014). All sampling equipment was cleaned One of the principal OM components consistently enriched in with acid (10% HCl) and rinsed in MilliQ before sampling. the SML are Transparent Exopolymer Particles (TEP) (Cunliffe In addition, all sampling devices were copiously rinsed with et al., 2009b; Wurl et al., 2011; Engel and Galgani, 2016), seawater from the respective depth when the sampling site was which are rich in carbohydrates and form by the aggregation of reached. dissolved precursors excreted by phytoplankton in the euphotic The ULW sample was collected with a LIMNOS water sampler zone (Chin et al., 1998; Passow, 2000; Passow et al., 2001; Engel (Hydro-bios) that had two acid cleaned (10% HCl) and MilliQ et al., 2004). Higher TEP formation rates in the SML, facilitated rinsed plastic bottles attached to it. A weight attached to the through wind shear and dilation of the surface water, have been LIMNOS sampler ensured that the bottles could not float to proposed as one explanation for the observed enrichment in TEP the surface during sampling. Since long waves rather than short (Wurl et al., 2011; Sun et al., 2018). Also, due to their natural breaking waves were most prominent, the depth of the LIMNOS positive buoyancy, when not ballasted by other particles sticking sampler could be adjusted manually by keeping a marker on the to them, TEP ascend through the water column and ultimately rope continuously at the surface during sampling. Sampling of end up at the SML (Azetsu-Scott and Passow, 2004). A second the ULW took about 30 s in total, keeping depth variations to a possible pathway of TEP from the water column to the SML is by minimum. bubble scavenging (Zhou et al., 1998). Next to rising bubbles, another potential transport mechanism Transparent Exopolymer Particles (TEP) for bacteria from the ULW to the SML could be ascending The abundance and area of TEP were measured microscopically particles (Agogué et al., 2005a; Joux et al., 2006) or more (Engel, 2009). Depending on the concentration of TEP, 10– specifically TEP (Azetsu-Scott and Passow, 2004). Bacteria readily 30 ml of the sample was filtered onto a 0.4 mm Nuclepore Frontiers in Microbiology| www.frontiersin.org 2 November 2018| Volume 9| Article 2699 fmicb-09-02699 November 15, 2018 Time: 13:25 # 3 Zäncker et al. Bacteria in the Peruvian SML FIGURE 1 | (A) Map of the cruise track of the RV Sonne in October 2015 during the SO243 cruise off the Peruvian coast.
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