Depth drives the distribution of microbial ecological functions in the coastal western Antarctic Peninsula.

The Antarctic marine environment is a dynamic ecosystem where microorganisms play an important role in key biogeochemical cycles. Despite the role that microbes play in this ecosystem, little is known about the genetic and metabolic diversity of Antarctic marine microbes. In this study we leveraged DNA samples collected by the Palmer Long Term Ecological Research (LTER) project to sequence shotgun metagenomes of 48 key samples collected across the marine ecosystem of the western Antarctic Peninsula (wAP). We developed an in silico metagenomics pipeline (iMAGine) for processing metagenomic data and constructing metagenome-assembled genomes (MAGs), identifying a diverse genomic repertoire related to the carbon, sulfur, and nitrogen cycles. A novel analytical approach based on gene coverage was used to understand the differences in microbial community functions across depth and region. Our results showed that microbial community functions were partitioned based on depth. Bacterial members harbored diverse genes for carbohydrate transformation, indicating the availability of processes to convert complex carbons into simpler bioavailable forms. We generated 137 dereplicated MAGs giving us a new perspective on the role of prokaryotes in the coastal wAP. In particular, the presence of mixotrophic prokaryotes capable of autotrophic and heterotrophic lifestyles indicated a metabolically flexible community, which we hypothesize enables survival under rapidly changing conditions. Overall, the study identified key microbial community functions and created a valuable sequence library collection for future Antarctic genomics research.

A surplus no more? Variation in krill availability impacts reproductive rates of Antarctic baleen whales.

The krill surplus hypothesis of unlimited prey resources available for Antarctic predators due to commercial whaling in the 20th century has remained largely untested since the 1970s. Rapid warming of the Western Antarctic Peninsula (WAP) over the past 50 years has resulted in decreased seasonal ice cover and a reduction of krill. The latter is being exacerbated by a commercial krill fishery in the region. Despite this, humpback whale populations have increased but may be at a threshold for growth based on these human-induced changes. Understanding how climate-mediated variation in prey availability influences humpback whale population dynamics is critical for focused management and conservation actions. Using an 8-year dataset (2013-2020), we show that inter-annual humpback whale pregnancy rates, as determined from skin-blubber biopsy samples (n = 616), are positively correlated with krill availability and fluctuations in ice cover in the previous year. Pregnancy rates showed significant inter-annual variability, between 29% and 86%. Our results indicate that krill availability is in fact limiting and affecting reproductive rates, in contrast to the krill surplus hypothesis. This suggests that this population of humpback whales may be at a threshold for population growth due to prey limitations. As a result, continued warming and increased fishing along the WAP, which continue to reduce krill stocks, will likely impact this humpback whale population and other krill predators in the region. Humpback whales are sentinel species of ecosystem health, and changes in pregnancy rates can provide quantifiable signals of the impact of environmental change at the population level. Our findings must be considered paramount in developing new and more restrictive conservation and management plans for the Antarctic marine ecosystem and minimizing the negative impacts of human activities in the region.

Inter-decadal variability of phytoplankton biomass along the coastal West Antarctic Peninsula.

The West Antarctic Peninsula (WAP) is a climatically sensitive region where periods of strong warming have caused significant changes in the marine ecosystem and food-web processes. Tight coupling between phytoplankton and higher trophic levels implies that the coastal WAP is a bottom-up controlled system, where changes in phytoplankton dynamics may largely impact other food-web components. Here, we analysed the inter-decadal time series of year-round chlorophyll-a (Chl) collected from three stations along the coastal WAP: Carlini Station at Potter Cove (PC) on King George Island, Palmer Station on Anvers Island and Rothera Station on Adelaide Island. There were trends towards increased phytoplankton biomass at Carlini Station (PC) and Palmer Station, while phytoplankton biomass declined significantly at Rothera Station over the studied period. The impacts of two relevant climate modes to the WAP, the El Niño-Southern Oscillation and the Southern Annular Mode, on winter and spring phytoplankton biomass appear to be different among the three sampling stations, suggesting an important role of local-scale forcing than large-scale forcing on phytoplankton dynamics at each station. The inter-annual variability of seasonal bloom progression derived from considering all three stations together captured ecologically meaningful, seasonally co-occurring bloom patterns which were primarily constrained by water-column stability strength. Our findings highlight a coupled link between phytoplankton and physical and climate dynamics along the coastal WAP, which may improve our understanding of overall WAP food-web responses to climate change and variability.This article is part of the theme issue 'The marine system of the West Antarctic Peninsula: status and strategy for progress in a region of rapid change'.

Winter and spring controls on the summer food web of the coastal West Antarctic Peninsula.

Understanding the mechanisms by which climate variability affects multiple trophic levels in food webs is essential for determining ecosystem responses to climate change. Here we use over two decades of data collected by the Palmer Long Term Ecological Research program (PAL-LTER) to determine how large-scale climate and local physical forcing affect phytoplankton, zooplankton and an apex predator along the West Antarctic Peninsula (WAP). We show that positive anomalies in chlorophyll-a (chl-a) at Palmer Station, occurring every 4-6 years, are constrained by physical processes in the preceding winter/spring and a negative phase of the Southern Annular Mode (SAM). Favorable conditions for phytoplankton included increased winter ice extent and duration, reduced spring/summer winds, and increased water column stability via enhanced salinity-driven density gradients. Years of positive chl-a anomalies are associated with the initiation of a robust krill cohort the following summer, which is evident in Adélie penguin diets, thus demonstrating tight trophic coupling. Projected climate change in this region may have a significant, negative impact on phytoplankton biomass, krill recruitment and upper trophic level predators in this coastal Antarctic ecosystem.

Aragonite precipitation by "proto-polyps" in coral cell cultures.

The mechanisms of coral calcification at the molecular, cellular and tissue levels are poorly understood. In this study, we examine calcium carbonate precipitation using novel coral tissue cultures that aggregate to form "proto-polyps". Our goal is to establish an experimental system in which calcification is facilitated at the cellular level, while simultaneously allowing in vitro manipulations of the calcifying fluid. This novel coral culturing technique enables us to study the mechanisms of biomineralization and their implications for geochemical proxies. Viable cell cultures of the hermatypic, zooxanthellate coral, Stylophora pistillata, have been maintained for 6 to 8 weeks. Using an enriched seawater medium with aragonite saturation state similar to open ocean surface waters (Ω(arag)~4), the primary cell cultures assemble into "proto-polyps" which form an extracellular organic matrix (ECM) and precipitate aragonite crystals. These extracellular aragonite crystals, about 10 µm in length, are formed on the external face of the proto-polyps and are identified by their distinctive elongated crystallography and X-ray diffraction pattern. The precipitation of aragonite is independent of photosynthesis by the zooxanthellae, and does not occur in control experiments lacking coral cells or when the coral cells are poisoned with sodium azide. Our results demonstrate that proto-polyps, aggregated from primary coral tissue culture, function (from a biomineralization perspective) similarly to whole corals. This approach provides a novel tool for investigating the biophysical mechanism of calcification in these organisms.

The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level.

Trait-based approaches to community structure are increasingly used in terrestrial ecology. We show that such an approach, augmented by a mechanistic analysis of trade-offs among functional traits, can be successfully used to explain community composition of marine phytoplankton along environmental gradients. Our analysis of literature on major functional traits in phytoplankton, such as parameters of nutrient-dependent growth and uptake, reveals physiological trade-offs in species abilities to acquire and utilize resources. These trade-offs, arising from fundamental relations such as cellular scaling laws and enzyme kinetics, define contrasting ecological strategies of nutrient acquisition. Major groups of marine eukaryotic phytoplankton have adopted distinct strategies with associated traits. These diverse strategies of nutrient utilization can explain the distribution patterns of major functional groups and size classes along nutrient availability gradients.

The mode and tempo of genome size evolution in eukaryotes.

Eukaryotic genome size varies over five orders of magnitude; however, the distribution is strongly skewed toward small values. Genome size is highly correlated to a number of phenotypic traits, suggesting that the relative lack of large genomes in eukaryotes is due to selective removal. Using phylogenetic contrasts, we show that the rate of genome size evolution is proportional to genome size, with the fastest rates occurring in the largest genomes. This trend is evident across the 20 major eukaryotic clades analyzed, indicating that over long time scales, proportional change is the dominant and universal mode of genome-size evolution in eukaryotes. Our results reveal that the evolution of eukaryotic genome size can be described by a simple proportional model of evolution. This model explains the skewed distribution of eukaryotic genome sizes without invoking strong selection against large genomes.

Use of hyperspectral remote sensing reflectance for detection and assessment of the harmful alga, Karenia brevis.

We applied two numerical methods to in situ hyperspectral measurements of remote sensing reflectance Rrs to assess the feasibility of remote detection and monitoring of the toxic dinoflagellate, Karenia brevis, which has been shown to exhibit unique absorption properties. First, an existing quasi-analytical algorithm was used to invert remote sensing reflectance spectra, Rrs(lambda), to derive phytoplankton absorption spectra, a(phi)Rrs(lambda). Second, the fourth derivatives of the a(phi)Rrs(lambda) spectra were compared to the fourth derivative of a reference K. brevis absorption spectrum by means of a similarity index (SI) analysis. Comparison of reflectance-derived a(phi) with filter pad measured a(phi) found them to agree well (R2=0.891; average percentage difference, 22.8%). A strong correlation (R2=0.743) between surface cell concentration and the SI was observed, showing the potential utility of SI magnitude as an indicator of bloom strength. A sensitivity analysis conducted to investigate the effects of varying levels of cell concentrations and colored dissolved organic matter (CDOM) on the efficacy of the quasi-analytical algorithm and SI found that a(phi)Rrs(lambda) could not be derived for very low cell concentrations and that, although it is possible to derive a(phi)Rrs(lambda) in the presence of high CDOM concentrations, CDOM levels influence the a(phi)Rrs(lambda) amplitude and shape. Results suggest that detection and mapping of K. brevis blooms based on hyperspectral measurements of Rrs are feasible.

Adaptive evolution of phytoplankton cell size.

We present a simple nutrient-phytoplankton-zooplankton (NPZ) model that incorporates adaptive evolution and allometric relations to examine the patterns and consequences of adaptive changes in plankton body size. Assuming stable environmental conditions, the model makes the following predictions. First, phytoplankton should evolve toward small sizes typical of picoplankton. Second, in the absence of grazers, nutrient concentration is minimized as phytoplankton reach their fitness maximum. Third, increasing nutrient flux tends to increase phytoplankton cell size in the presence of phytoplankton-zooplankton coevolution but has no effect in the absence of zooplankton. Fourth, phytoplankton reach their fitness maximum in the absence of grazers, and the evolutionary nutrient-phytoplankton system has a stable equilibrium. In contrast, phytoplankton may approach their fitness minimum in the evolutionary NPZ system where phytoplankton and zooplankton are allowed to coevolve, which may result in oscillatory (unstable) dynamics of the evolutionary NPZ system, compared with the otherwise stable nonevolutionary NPZ system. These results suggest that evolutionary interactions between phytoplankton and zooplankton may have contributed to observed changes in phytoplankton sizes and associated biogeochemical cycles over geological time scales.

Climatically driven macroevolutionary patterns in the size of marine diatoms over the Cenozoic.

Numerous taxonomic groups exhibit an evolutionary trajectory in cell or body size. The size structure of marine phytoplankton communities strongly affects food web structure and organic carbon export into the ocean interior, yet macroevolutionary patterns in the size structure of phytoplankton communities have not been previously investigated. We constructed a database of the size of the silica frustule of the dominant fossilized marine planktonic diatom species over the Cenozoic. We found that the minimum and maximum sizes of the diatom frustule have expanded in concert with increasing species diversity. In contrast, the mean area of the diatom frustule is highly correlated with oceanic temperature gradients inferred from the delta18O of foraminiferal calcite, consistent with the hypothesis that climatically induced changes in oceanic mixing have altered nutrient availability in the euphotic zone and driven macroevolutionary shifts in the size of marine pelagic diatoms through the Cenozoic.

Continuous hyperspectral absorption measurements of colored dissolved organic material in aquatic systems.

The majority of organic carbon in the oceans is present as dissolved organic matter (DOM); therefore understanding the distribution and dynamics of DOM is central to understanding global carbon cycles. Describing the time-space variability in colored dissolved organic matter (CDOM) has been difficult, as standard spectrophotometric methods for CDOM determination are laborious and susceptible to methodological biases. Previously, measurements of CDOM absorption in discrete water samples by use of a liquid-waveguide capillary cell (LWCC) compared favorably with measurements made with a benchtop spectrophotometer. Given this, we focused on automating the LWCC technique to improve our spatial and temporal sampling capabilities for CDOM. We found strong correlations between CDOM absorption spectra collected from discrete water samples using standard methods and selected corresponding CDOM spectra collected by the automated LWCC system. The near-continuous measurements by the LWCC system made it possible to map the temporal, spatial, and spectral variability of CDOM absorption along the ship track.