Photosynthetic picoeukaryote community structure in the South East Pacific Ocean encompassing the most oligotrophic waters on Earth

Abstract

Photosynthetic picoeukaryotes (PPEs), comprising organisms < 3 mum in size, are important primary producers in marine food webs and include representatives from all known algal lineages. Little is known, however, regarding the composition and distribution of PPE communities, particularly at large spatial scales, or in relation to the underlying biotic and abiotic factors that influence this structure. Here, we analysed PPE community structure along a transect in the South East Pacific Ocean (BIOSOPE cruise) that encompassed a large trophic gradient, including hyper-oligotrophic waters in the South Pacific Gyre (SPG), considered to be some of the 'clearest' natural waters on Earth. Using dot blot hybridizations with 16S rRNA oligonucleotide probes, we established that the PPE community was dominated by members of the classes Prymnesiophyceae and Chrysophyceae throughout the transect. Moreover, clone library construction followed by phylogenetic analysis of sequenced clones revealed several novel 16S rRNA gene lineages, including new clades of prymnesiophytes (designated Prym 16S-III) and prasinophytes (Pras 16S-VIII). Pras 16S-VIII was found at all five stations at which clone libraries were constructed, representing a range of trophic conditions, including the South Pacific Gyre, suggesting members of this clade have a broad distribution in this part of the South East Pacific at least. In contrast, Prym 16S-III sequences were largely restricted to oligotrophic stations of the SPG. Subsequent multivariate statistical analyses showed that, within the measured factors, chemical and biological factors seem to influence PPE community structure more than physical parameters. However, more than 50% of the variation in distribution of PPE classes remained unexplained.

Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean

“…Moreover, the majority of these sequences were taxonomically affiliated with lineages with no close cultured counterpart. While prymnesiophytes appear widespread in most mesotrophic and oligotophic waters (Bidigare and Ondrusek, 1996;Moon-van der Staay et al, 2000;Díez et al, 2001;Wilmotte et al, 2002;Fuller et al, 2006b;Lepère et al, 2009) and can contribute from 30% to 50% of total photosynthetic standing stock across the world ocean (Liu et al, 2009), cultured representatives of the size fractions reported here are still rare. The prymnesiophytes observed in this study are likely not calcified as shown both by microscopy ( Figure 5a) and their flow cytometry signature (that is, their 901 light scatter was similar to other eukaryotic cells) (Supplementary Figure 1) reinforcing the assertion that these prymnesiophytes include novel groups.…”

“…Plastid 16S rRNA gene sequences obtained through clone library construction of sorted Euk-B cells allowed us to ascertain more accurately the composition of the Euk-B group. Subsequent phylogenetic analysis (Figure 6) showed that these prymnesiophytes were closely related to environmental sequences retrieved from the southeast Pacific Ocean encompassing some of the most oligotrophic waters on earth (Lepère et al, 2009) suggesting these lineages have a wide geographic distribution. Moreover, the majority of these sequences were taxonomically affiliated with lineages with no close cultured counterpart.…”

“…K: values 4 90%; J: 70-90%; values o70% are not shown. Environmental sequences are as follows: Solas: clones from the D326 cruise; AS: clones from the Arabian Sea (Fuller et al, 2006a); MC and MAMA: clones from the Gulf of Naples (McDonald et al, 2007); DYF: clones from the northwest Mediterranean Sea Dyfamed station (Marie et al, 2006); Biosope: clones from the southeast Pacific Ocean (Lepère et al, 2009).…”

“…However, the chrysophytes observed by microscopy and TSA-FISH here had two chloroplasts, no apparent siliceous deposits in the outer membrane (that is, their 901 light scatter was similar to other eukaryotic cells) and were smaller than 2.5 mm (Figure 5b). Moreover, plastid 16S rRNA gene sequences of photosynthetic chrysophytes have recently been reported from various marine environments (Fuller et al, 2006a, b;McDonald et al, 2007;Lepère et al, 2009) highlighting the potentially wide distribution and ecological importance of this class. Furthermore, 18S rRNA gene sequences of marine chrysophytes forming new groups without cultured representatives and comprising putative photosynthetic organisms have also been retrieved in several recent studies (Worden and Not, 2008;Shi et al, 2009).…”

“…Moreover, studies based on size-fractionated pigment analysis also suggest a wide distribution of these small photosynthetic eukaryotes (Latasa and Bidigare, 1998;Wright et al, 2009). Recent progress using molecular approaches has begun to reveal their diversity (Moon-van der Staay et al, 2000;Díez et al, 2001;Vaulot et al, 2008;Worden and Not, 2008) showing a dominance of prymnesiophytes, pelagophytes and prasinophytes in marine environments (for example, see Moon-van der Staay et al, 2001;Romari and Vaulot, 2004;Not et al, 2004;Fuller et al, 2006a, b;Viprey et al, 2008;Liu et al, 2009) and lately of chrysophytes (Fuller et al, 2006b;McDonald et al, 2007;Lepère et al, 2009). However, we still have a poor understanding of the phylogenetic affiliation of the smallest cells (for example, see Liu et al, 2010), and particularly in directly linking taxonomic identity with 14 C primary production measurements.…”