Molecular underpinnings and biogeochemical consequences of enhanced diatom growth in a warming Southern Ocean

Abstract

<jats:title>Abstract</jats:title><jats:p>The Southern Ocean (SO) harbours some of the most intense phytoplankton blooms on Earth. Changes in temperature and iron availability are expected to alter the intensity of SO phytoplankton blooms, but little is known about how environmental change will influence community composition and downstream biogeochemical processes. We performed experimental manipulations on surface ocean microbial communities from McMurdo Sound in the Ross Sea, with and without iron addition, at −0.5 °C, 3 °C, and 6 °C. We then examined nutrient uptake patterns as well as the growth and molecular responses of two dominant diatoms, <jats:italic>Fragilariopsis</jats:italic> and <jats:italic>Pseudo-nitzschia</jats:italic>, to these conditions. We found that nitrate uptake and primary productivity were elevated at increased temperature in the absence of iron addition, and were even greater at high temperature with added iron. <jats:italic>Pseudo-nitzschia</jats:italic> became more abundant under increased temperature without added iron, while <jats:italic>Fragilariopsis</jats:italic> required additional iron to benefit from warming. We attribute the apparent advantage <jats:italic>Pseudo-nitzschia</jats:italic> shows under warming to upregulation of iron-conserving photosynthetic processes, utilization of iron-economic nitrogen assimilation mechanisms, and increased iron uptake and storage. These data identify important molecular and physiological differences between dominant diatom groups and add to the growing body of evidence for <jats:italic>Pseudo-nitzschia</jats:italic>’s increasingly important role in warming SO ecosystems. This study also suggests that temperature-driven shifts in SO phytoplankton assemblages may increase utilization of the vast pool of excess nutrients in iron-limited SO surface waters, and thereby influence global nutrient distributions and carbon cycle.</jats:p><jats:sec><jats:title>Significance Statement</jats:title><jats:p>Phytoplankton assemblages contribute to the Southern Ocean’s ability to absorb atmospheric CO<jats:sub>2</jats:sub>, form the base of marine food webs, and shape the global distribution of macronutrients. Anthropogenic climate change is altering the SO environment, yet we do not fully understand how resident phytoplankton will react to this change. By comparing the responses of two prominent SO diatom groups to changes in temperature and iron in a natural community, we find that one group, <jats:italic>Pseudo-nitzschia</jats:italic>, grows better under warmer low-iron conditions by managing cellular iron demand and efficiently increasing photosynthetic capacity. This ability to grow and draw down nutrients in the face of warming, regardless of iron availability, may have major implications for ocean ecosystems and global nutrient and carbon cycles.</jats:p></jats:sec>

Comparative transcriptomics unveil distinctive metabolic pathway of phosphonate utilization by diatom Phaeodactylum tricornutum

“…4b, Supplementary Table S8). Through searching the Southern Ocean (SO) diatom assemblage transcriptome database [50], we also identified abundant transcript expression of four selected genes (Supplementary Table S9) in diatom species shown in Fig. 3e.…”

Proteomic traits vary across taxa in a coastal Antarctic phytoplankton bloom

“…We used metagenomics and metatranscriptomics to obtain reference databases of potential proteins for metaproteomics. We additionally used a database assembled from a similarly processed metatranscriptomic incubation experiment [28], conducted with source water from the January 15, 2015 time point (these samples were collected on a 0.2um Sterivex filter and processed as previously described).…”

“…The MCL algorithm was subsequently implemented using default parameters. MCL Clusters were then assigned consensus annotations based on KEGG, KO, KOG, KOG class, Pfam, TIGRfam, EC, GO, annotation enrichment [28,32]. Proteins were assigned to coarse-grained protein pools (ribosomal and photosynthetic proteins) based on these annotations.…”

“…In order to make these databases (Table 1), we performed three separate assemblies on 1) the metagenomic reads (from samples GOS-927, GOS-930, GOS-933 and GOS-935), 2) metatranscriptomic reads (from samples GOS-927, GOS-930, GOS-933 and GOS-935) and 3) metatranscriptomic reads from a concurrent metatranscriptomic experiment, started at the location where GOS-933 was taken [28]. Database configurations were created by subsetting from these assemblies.…”

“…ORFs were subsetted from the metagenomic and metatranscriptomic assemblies as above. The fourth and fifth configurations are from the concurrent metatranscriptomic experiment [28]. The fourth configuration ('metatranscriptome experiment (T0)') was the metatranscriptome of the in situ microbial community (i.e.…”