Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the South East Pacific Ocean

Picophytoplankton, including photosynthetic picoeukaryotes (PPE) and unicellular cyanobacteria, are important contributors to plankton biomass and primary productivity. In this study, phytoplankton composition and rates of carbon fixation were examined across a large trophic gradient in the South East Pacific Ocean (SEP) using a suite of approaches: photosynthetic pigments, rates of C-primary productivity, and phylogenetic analyses of partial 18S rRNA genes PCR amplified and sequenced from flow cytometrically sorted cells. While phytoplankton >10 lm (diatoms and dinoflagellates) were prevalent in the upwelling region off the Chilean coast, picophytoplankton consistently accounted for 55–92% of the total chlorophyll a inventories and >60% of C-primary productivity throughout the sampling region. Estimates of rates of C-primary productivity derived from flow cytometric sorting of radiolabeled cells revealed that the contributions of PPE and Prochlorococcus to euphotic zone depth-integrated picoplankton productivity were nearly equivalent (ranging 36–57%) along the transect, with PPE comprising a larger share of picoplankton productivity than cyanobacteria in the well-lit (>15% surface irradiance) region compared with in the lower regions (1–7% surface irradiance) of the euphotic zone. 18S rRNA gene sequence analyses revealed the taxonomic identities of PPE; e.g., Mamiellophyceae (Ostreococcus) were the dominant PPE in the upwelling-influenced waters, while members of the Chrysophyceae, Prymnesiophyceae, Pelagophyceae, and Prasinophyceae Clades VII and IX flourished in the oligotrophic South Pacific Subtropical Gyre. Our results suggest that, despite low numerical abundance in comparison to cyanobacteria, diverse members of PPE are significant contributors to carbon cycling across biogeochemically distinct regions of the SEP. Primary production in the ocean accounts for nearly half of the net global carbon fixation and a substantial fraction of this productivity occurs in the oligotrophic subtropical gyres (Field et al. 1998; Carr et al. 2006). Picophytoplankton (typically defined as microorganisms <2–3 lm) include unicellular cyanobacteria and photosynthetic picoeukaryotes (PPE) and are significant contributors to productivity and plankton biomass, particularly in the subtropical ocean gyres (Sieburth et al. 1978; Li 1994; Massana 2011). Due to their numerical dominance, Prochlorococcus and Synechococcus have long been thought to be responsible for a majority of the picophytoplankton productivity in oligotrophic waters. However, several studies have reported that, despite generally low abundances, diverse members of PPE can contribute significantly to biomass and primary production due to their larger cell biovolumes and rapid growth rates (Li 1994; Worden et al. 2004; Jardillier et al. 2010). For example, Worden et al. (2004) estimated that despite small differences in their cell diameters (PPE5 2.0 lm, Prochlorococcus5 0.7 lm, and Synechococcus5 1.1 lm), PPE carbon content was 6.5-fold to 14-fold greater than that of pico-cyanobacteria. Combined, PPE’s larger biovolume and rapid growth rates indicate that PPE can be active and significant components of picophytoplankton population dynamics in the ocean. *Correspondence: [email protected] This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. 806 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 61, 2016, 806–824 VC 2016 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10255 Photosynthetic picoeukaryotes include taxonomically diverse populations, with members scattered widely across many branches of the eukaryotic tree of life (Baldauf 2003; Vaulot et al. 2008; Massana 2011). Studies examining PPE diversity in various regions of the world’s oceans show that members of the prasinophyte algae (Mamiellophyceae) have been found to be abundant in nutrient-enriched, coastal regions (Guillou et al. 2004; Romari and Vaulot 2004; Worden 2006), while groups of uncultured prymnesiophytes, chrysophytes, and pelagophytes are often more dominant in open ocean waters (Fuller et al. 2006; Shi et al. 2009; Cuvelier et al. 2010). The cosmopolitan distribution of PPE may reflect their metabolic flexibility. Many PPE taxa appear capable of mixotrophy, combining photosynthetic growth with phagotrophic consumption of other picoplankton for nutrition, thereby complicating characterization of the ecological roles of these organisms (Zubkov and Tarran 2008; Caron et al. 2009; Hartmann et al. 2012). To date, whether or how variability in the composition of picophytoplankton assemblages influences productivity remains unclear. For example, a recent study in the Atlantic Ocean concluded that biomass-specific rates of primary production by PPE appeared largely unaffected by changes in the phylogenetic structure of PPE assemblages (Grob et al. 2011). In this study, we examined spatial variation in PPE diversity and contributions to productivity across diverse habitats of the South East Pacific Ocean (SEP). This study was conducted as part of the research expedition Biogeochemical Gradients: Role in Arranging Planktonic Assemblages (BiG RAPA), which focused on examining microplankton ecology in the SEP. We sampled biogeochemically distinct regions of the SEP that spanned the productive waters in the permanent upwelling zone off the coast of Chile to the oligotrophic waters of the South Pacific Subtropical Gyre (SPSG). We utilized a suite of approaches to characterize spatial variability in PPE population structure, including photosynthetic pigment-based analyses and assessment of 18S rRNA genes derived from flow cytometrically sorted PPE cells. In addition, we evaluated spatial changes in size-fractionated and PPE group-specific rates of primary productivity. Collectively, we aimed to evaluate the contributions of specific picophytoplankton to plankton biomass and the roles they play in productivity across various nutrient regimes.