Biogeography of Heterotrophic Flagellate Populations Indicates the Presence of Generalist and Specialist Taxa in the Arctic Ocean

Abstract

Heterotrophic marine flagellates (HF) are ubiquitous in the world's oceans and represented in nearly all branches of the domain Eukaryota. However, the factors determining distributions of major taxonomic groups are poorly known. The Arctic Ocean is a good model environment for examining the distribution of functionally similar but phylogenetically diverse HF because the physical oceanography and annual ice cycles result in distinct environments that could select for microbial communities or favor specific taxa. We reanalyzed new and previously published high-throughput sequencing data from multiple studies in the Arctic Ocean to identify broad patterns in the distribution of individual taxa. HF accounted for fewer than 2% to over one-half of the reads from the water column and for up to 60% of reads from ice, which was dominated by Cryothecomonas. In the water column, many HF phylotypes belonging to Telonemia and Picozoa, uncultured marine stramenopiles (MAST), and choanoflagellates were geographically widely distributed. However, for two groups in particular, Telonemia and Cryothecomonas, some species level taxa showed more restricted distributions. For example, several phylotypes of Telonemia favored open waters with lower nutrients such as the Canada Basin and offshore of the Mackenzie Shelf. In summary, we found that while some Arctic HF were successful over a range of conditions, others could be specialists that occur under particular conditions. We conclude that tracking species level diversity in HF not only is feasible but also provides a potential tool for understanding the responses of marine microbial ecosystems to rapidly changing ice regimes. Heterotrophic flagellates (HF) have a central role in marine food webs, particularly in the Arctic, where they can control phytoplankton biomass (1). Modeling studies indicate that they likely consume the majority of bacterial biomass in this region (2). In other marine environments, they have been found to be more important than viral lysis (3) or ciliate grazers (4) for controlling bacterial concentrations. HF range from pico-to nanosized cells (0.8 to 20 m) and are phylogenetically diverse, with representatives in most branches of the Eukaryota tree. Because taxon-specific differences in feeding behavior, population dynamics, and life histories may be important over broad ecosystem scales (5), the identification and quantification of the diverse groups can add substantially to our understanding of marine ecosystem function. However, HF taxa often have few diagnostic morphological features that enable easy identification (6) and microscopy-based studies rarely differentiate between HF taxonomic groups. Molecular approaches, such as cloning and amplicon sequencing, have provided additional information on the deep phylogenetic diversity of HF, especially in the Arctic (7). More recently, highthroughput multiplex tag sequencing of hypervariable regions of the 18S rRNA gene has become commonplace (8, 9). This is considered a semiquantitative method for retrievin...

Strong Seasonality of Marine Microbial Eukaryotes in a High-Arctic Fjord (Isfjorden, in West Spitsbergen, Norway)

“…The filter size used in this study should remove most of the Ciliophora described, since these are generally larger than 10 m (94). Ciliates are, however, commonly detected on small-pore-sized filters (14,63), probably because they have flexible cells that are able to pass through (89). The high OTU richness identified among the Alveolata could result from a lack of homogenization of their rDNA gene copies (95), although we believe that we have minimized the effects of intracellular variability, PCR errors, and sequencing errors by using a 97% cutoff during clustering.…”

Diversity of planktonic microorganisms in the Arctic Ocean

“…A number of these studies investigated Arctic Bacteria (Ferrari and Hollibaugh, 1999;Bano and Hollibaugh, 2002;Pommier et al, 2007;Malmstrom et al, 2007;Garneau et al, 2006;Kellogg and Deming, 2009), Archaea (Bano et al, 2004;Galand et al, 2006Galand et al, , 2008a and eukaryotic microbes Potvin and Lovejoy, 2009;Terrado et al, 2011). Short reads from newer high throughput sequencing technology can then be mapped onto phylogenetic trees providing finer resolution, however in the Arctic this approach has only recently been applied to microbial eukaryotic communities (Thaler and Lovejoy, 2015).…”

Seasonal and Interannual Changes in Ciliate and Dinoflagellate Species Assemblages in the Arctic Ocean (Amundsen Gulf, Beaufort Sea, Canada)

“…To investigate the OTUs that contributed to the changes in July 2008 for the interannual data (see Section Results), the remaining abundant "Other Ciliate" OTUs were searched for in NCBI and their most similar nearly full length 18S rRNA gene sequences were used to construct reference trees as in Thaler and Lovejoy (2015). Then, the abundant but unclassified ciliate OTUs were then mapped back onto the reference trees using EPA RAxML v.8 (Stamatakis, 2014).…”

“…All PC filters were placed in 2-mL cryovials. Prior to 2010, DNA was preserved by adding 1.8 mL of lysis buffer to the Sterivex units (0.2-3 µm fraction) and cryovials (3-50 µm fraction), and RNA was preserved in RLT buffer (Qiagen) as in Terrado et al (2011) and Thaler and Lovejoy (2015). Samples were either frozen immediately at −80 • C or placed in liquid nitrogen after adding buffer.…”