Abstract
The tropical marine environments of northern Australia encompasses a diverse range of geomorphological and oceanographic conditions and high levels of productivity and nitrogen fixation. However, efforts to characterize phytoplankton assemblages in these waters have been restricted to studies using microscopic and pigment analyses, leading to the current consensus that this region is dominated by large diatoms, dinoflagellates, and the marine cyanobacterium Trichodesmium. During an oceanographic transect from the Arafura Sea through the Torres Strait to the Coral Sea, we characterized prokaryotic and eukaryotic phytoplankton communities in surface waters using a combination of flow cytometry and Illumina based 16S and 18S ribosomal RNA amplicon sequencing. Similar to observations in other marine regions around Australian, phytoplankton assemblages throughout this entire region were rich in unicellular picocyanobacterial primary producers while picoeukaryotic phytoplankton formed a consistent, though smaller proportion of the photosynthetic biomass. Major taxonomic groups displayed distinct biogeographic patterns linked to oceanographic and nutrient conditions. Unicellular picocyanobacteria dominated in both flow cytometric abundance and carbon biomass, with members of the Synechococcus genus dominating in the shallower Arafura Sea and Torres Strait where chlorophyll a was relatively higher (averaging 0.4 ± 0.2 mg m-3), and Prochlorococcus dominating in the oligotrophic Coral Sea where chlorophyll a averaged 0.13 ± 0.07 mg m-3. Consistent with previous microscopic and pigment-based observations, we found from sequence analysis that a variety of diatoms (Bacillariophyceae) exhibited high relative abundance in the Arafura Sea and Torres Strait, while dinoflagellates (Dinophyceae) and prymnesiophytes (Prymnesiophyceae) were more abundant in the Coral Sea. Ordination analysis identified temperature, nutrient concentrations and water depth as key drivers of the region’s assemblage composition. This is the first molecular and flow cytometric survey of the abundance and diversity of both prokaryotic and picoeukaryotic phytoplankton in this region, and points to the need to include the picocyanobacterial populations as an essential oceanic variable for sustained monitoring in order to better understand the health of these important coastal waters as global oceans change.
Highlights
A combination of prokaryotic and microbial eukaryotic phytoplankton contribute to photosynthetic abundance, biomass and primary production in the oligotrophic and mesotrophic oceans from the temperate latitudes to the tropics
4 mL of seawater was fixed for 1 h at 41◦C with 1% paraformaldehyde before being snap frozen in liquid nitrogen and stored at −80◦C (Marie et al, 1997) for later flow cytometry analysis
In addition to separating the chloroplast 16S ribosomal RNA (rRNA) gene operational taxonomic units (OTUs) into their own dataset for analysis of the eukaryotic phytoplankton that might not have been identified properly in the eukaryotic phytoplankton 18S rRNA gene OTU dataset, we focused our analysis of the 16S rRNA gene OTUs only on the cyanobacteria by removing all non-phototrophic prokaryotic OTUs including the few known non-photosynthetic cyanobacteria, Melainabacteria, ML635J-21 (Soo et al, 2014; Monchampa et al, 2016), and Candidatus A. thalassa (Thompson et al, 2012)
Summary
A combination of prokaryotic and microbial eukaryotic phytoplankton contribute to photosynthetic abundance, biomass and primary production in the oligotrophic and mesotrophic oceans from the temperate latitudes to the tropics. Photosynthetic microbial eukaryotes account for a significant fraction of primary production in temperate mesotrophic waters but can be important components of subtropical ocean assemblages (Vaulot et al, 2008; Jardillier et al, 2010; Buitenhuis et al, 2012). They are ubiquitous in the surface oceans (Jürgens and Massana, 2008) and their substantial biodiversity contributes to marine ecosystem stability, resilience and function (Loreau et al, 2001; Wardle et al, 2004). Understanding the contribution of photosynthetic prokaryotes to the trophic cascade of energy and matter in more productive waters is being recognized as critical to better understanding the health of the oceans (Miloslavich et al, 2018; Ullah et al, 2018)
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