An under-ice bloom of mixotrophic haptophytes in low nutrient and freshwater-influenced Arctic waters.

The pelagic spring bloom is essential for Arctic marine food webs, and a crucial driver of carbon transport to the ocean depths. A critical challenge is understanding its timing and magnitude, to predict its changes in coming decades. Spring bloom onset is typically light-limited, beginning when irradiance increases or during ice breakup. Here we report an acute 9-day under-ice algal bloom in nutrient-poor, freshwater-influenced water under 1-m thick sea ice. It was dominated by mixotrophic brackish water haptophytes (Chrysochromulina/ Prymnesium) that produced 5.7 g C m-2 new production. This estimate represents about half the annual pelagic production, occurring below sea ice with a large contribution from the mixotrophic algae bloom. The freshwater-influenced, nutrient-dilute and low light environment combined with mixotrophic community dominance implies that phagotrophy played a critical role in the under-ice bloom. We argue that such blooms dominated by potentially toxic mixotrophic algae might become more common and widespread in the future Arctic Ocean.

Mapping the in situ microspatial distribution of ice algal biomass through hyperspectral imaging of sea-ice cores.

Ice-associated microalgae make a significant seasonal contribution to primary production and biogeochemical cycling in polar regions. However, the distribution of algal cells is driven by strong physicochemical gradients which lead to a degree of microspatial variability in the microbial biomass that is significant, but difficult to quantify. We address this methodological gap by employing a field-deployable hyperspectral scanning and photogrammetric approach to study sea-ice cores. The optical set-up facilitated unsupervised mapping of the vertical and horizontal distribution of phototrophic biomass in sea-ice cores at mm-scale resolution (using chlorophyll a [Chl a] as proxy), and enabled the development of novel spectral indices to be tested against extracted Chl a (R2 ≤ 0.84). The modelled bio-optical relationships were applied to hyperspectral imagery captured both in situ (using an under-ice sliding platform) and ex situ (on the extracted cores) to quantitatively map Chl a in mg m-2 at high-resolution (≤ 2.4 mm). The optical quantification of Chl a on a per-pixel basis represents a step-change in characterising microspatial variation in the distribution of ice-associated algae. This study highlights the need to increase the resolution at which we monitor under-ice biophysical systems, and the emerging capability of hyperspectral imaging technologies to deliver on this research goal.

Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier.

Conserving additional energy from sunlight through bacteriochlorophyll (BChl)-based reaction center or proton-pumping rhodopsin is a highly successful life strategy in environmental bacteria. BChl and rhodopsin-based systems display contrasting characteristics in the size of coding operon, cost of biosynthesis, ease of expression control, and efficiency of energy production. This raises an intriguing question of whether a single bacterium has evolved the ability to perform these two types of phototrophy complementarily according to energy needs and environmental conditions. Here, we report four Tardiphaga sp. strains (Alphaproteobacteria) of monophyletic origin isolated from a high Arctic glacier in northeast Greenland (81.566° N, 16.363° W) that are at different evolutionary stages concerning phototrophy. Their >99.8% identical genomes contain footprints of horizontal operon transfer (HOT) of the complete gene clusters encoding BChl- and xanthorhodopsin (XR)-based dual phototrophy. Two strains possess only a complete XR operon, while the other two strains have both a photosynthesis gene cluster and an XR operon in their genomes. All XR operons are heavily surrounded by mobile genetic elements and are located close to a tRNA gene, strongly signaling that a HOT event of the XR operon has occurred recently. Mining public genome databases and our high Arctic glacial and soil metagenomes revealed that phylogenetically diverse bacteria have the metabolic potential of performing BChl- and rhodopsin-based dual phototrophy. Our data provide new insights on how bacteria cope with the harsh and energy-deficient environment in surface glacier, possibly by maximizing the capability of exploiting solar energy.IMPORTANCE Over the course of evolution for billions of years, bacteria that are capable of light-driven energy production have occupied every corner of surface Earth where sunlight can reach. Only two general biological systems have evolved in bacteria to be capable of net energy conservation via light harvesting: one is based on the pigment of (bacterio-)chlorophyll and the other is based on proton-pumping rhodopsin. There is emerging genomic evidence that these two rather different systems can coexist in a single bacterium to take advantage of their contrasting characteristics in the number of genes involved, biosynthesis cost, ease of expression control, and efficiency of energy production and thus enhance the capability of exploiting solar energy. Our data provide the first clear-cut evidence that such dual phototrophy potentially exists in glacial bacteria. Further public genome mining suggests this understudied dual phototrophic mechanism is possibly more common than our data alone suggested.

Photobiology of sea ice algae during initial spring growth in Kangerlussuaq, West Greenland: insights from imaging variable chlorophyll fluorescence of ice cores.

We undertook a series of measurements of photophysiological parameters of sea ice algae over 12 days of early spring growth in a West Greenland Fjord, by variable chlorophyll fluorescence imaging. Imaging of the ice-water interface showed the development of ice algae in 0.3-0.4 mm wide brine channels between laminar ice crystals in the lower 4-6 mm of the ice, with a several-fold spatial variation in inferred biomass on cm scales. The maximum quantum yield of photosynthesis, F(v) /F(m), was initially low (~0.1), though this increased rapidly to ~0.5 by day 6. Day 6 also saw the onset of biomass increase, the cessation of ice growth and the time at which brine had reached <50 psu and >-2 °C. We interpret this as indicating that the establishment of stable brine channels at close to ambient salinity was required to trigger photosynthetically active populations. Maximum relative electron transport rate (rETR(max)), saturation irradiance (E(k)) and photosynthetic efficiency (α) had also stabilised by day 6 at 5-6 relative units, ~30 µmol photons m⁻² s⁻¹ and 0.4-0.5 µmol photons m⁻²s⁻¹, respectively. E(k) was consistent with under-ice irradiance, which peaked at a similar value, confirming that daytime irradiance was adequate to facilitate photosynthetic activity throughout the study period. Photosynthetic parameters showed no substantial differences with depth within the ice, nor variation between cores or brine channels suggesting that during this early phase of ice algal growth cells were unaffected by gradients of environmental conditions within the ice. Variable chlorophyll fluorescence imaging offers a tool to determine how this situation may change over time and as brine channels and algal populations evolve.