John A. E. Gibson

Antarctic terrestrial life – challenging the history of the frozen continent?

Antarctica is a continent locked in ice, with almost 99.7% of current terrain covered by permanent ice and snow, and clear evidence that, as recently as the Last Glacial Maximum (LGM), ice sheets were both thicker and much more extensive than they are now. Ice sheet modelling of both the LGM and estimated previous ice maxima across the continent give broad support to the concept that most if not all currently ice‐free ground would have been overridden during previous glaciations. This has given rise to a widely held perception that all Mesozoic (pre‐glacial) terrestrial life of Antarctica was wiped out by successive and deepening glacial events. The implicit conclusion of such destruction is that most, possibly all, contemporary terrestrial life has colonised the continent during subsequent periods of glacial retreat. However, several recently emerged and complementary strands of biological and geological research cannot be reconciled comfortably with the current reconstruction of Antarctic glacial history, and therefore provide a fundamental challenge to the existing paradigms. Here, we summarise and synthesise evidence across these lines of research. The emerging fundamental insights corroborate substantial elements of the contemporary Antarctic terrestrial biota being continuously isolated in situ on a multi‐million year, even pre‐Gondwana break‐up timescale. This new and complex terrestrial Antarctic biogeography parallels recent work suggesting greater regionalisation and evolutionary isolation than previously suspected in the circum‐Antarctic marine fauna. These findings both require the adoption of a new biological paradigm within Antarctica and challenge current understanding of Antarctic glacial history. This has major implications for our understanding of the key role of Antarctica in the Earth System.

Virophage control of antarctic algal host–virus dynamics

Viruses are abundant ubiquitous members of microbial communities and in the marine environment affect population structure and nutrient cycling by infecting and lysing primary producers. Antarctic lakes are microbially dominated ecosystems supporting truncated food webs in which viruses exert a major influence on the microbial loop. Here we report the discovery of a virophage (relative of the recently described Sputnik virophage) that preys on phycodnaviruses that infect prasinophytes (phototrophic algae). By performing metaproteogenomic analysis on samples from Organic Lake, a hypersaline meromictic lake in Antarctica, complete virophage and near-complete phycodnavirus genomes were obtained. By introducing the virophage as an additional predator of a predator–prey dynamic model we determined that the virophage stimulates secondary production through the microbial loop by reducing overall mortality of the host and increasing the frequency of blooms during polar summer light periods. Virophages remained abundant in the lake 2 y later and were represented by populations with a high level of major capsid protein sequence variation (25–100% identity). Virophage signatures were also found in neighboring Ace Lake (in abundance) and in two tropical lakes (hypersaline and fresh), an estuary, and an ocean upwelling site. These findings indicate that virophages regulate host–virus interactions, influence overall carbon flux in Organic Lake, and play previously unrecognized roles in diverse aquatic ecosystems.

Dimethylsulfide and the algaPhaeocystis pouchetii in antarctic coastal waters

The concentrations of dimethylsulfide (DMS), dimethylsulfoniopropionate (DMSP) and dimethylsulfoxide (DMSO) were measured in water collected from the Southern Ocean 10 km offshore from Davis Station, Antarctica, during the period May 1987 to January 1988, inclusive. During winter and spring, when the sea-ice was up to 1.9 m thick, DMS, DMSP and DMSO concentrations were low (0.2 to 1.5 nM), as were phytoplankton numbers. The maximum concentration of the sulfur compounds generally occurred in the top 10 m of the water column. DMS levels rose dramatically from early December onwards, reaching a peak of 290 nM at a depth of 15 m in January. This concentration is higher than reported elsewhere in the ocean. These high concentrations occurred at the same time as a bloom of the algaPhaeocystis pouchetii. A significant correlation occurred between DMS concentration and cell numbers of the alga. The ratio of DMS concentration to the number of cells of the alga was considerably higher than reported for blooms of this species elsewhere in the ocean. Up to 10% of the total global flux of DMS to the atmosphere may emanate from antarctic seas.

Prokaryotic Metabolic Activity and Community Structure in Antarctic Continental Shelf Sediments

ABSTRACT The prokaryote community activity and structural characteristics within marine sediment sampled across a continental shelf area located off eastern Antarctica (66°S, 143°E; depth range, 709 to 964 m) were studied. Correlations were found between microbial biomass and aminopeptidase and chitinase rates, which were used as proxies for microbial activity. Biomass and activity were maximal within the 0- to 3-cm depth range and declined rapidly with sediment depths below 5 cm. Most-probable-number counting using a dilute carbohydrate-containing medium recovered 1.7 to 3.8% of the sediment total bacterial count, with mostly facultatively anaerobic psychrophiles cultured. The median optimal growth temperature for the sediment isolates was 15°C. Many of the isolates identified belonged to genera characteristic of deep-sea habitats, although most appear to be novel species. Phospholipid fatty acid (PLFA) and isoprenoid glycerol dialkyl glycerol tetraether analyses indicated that the samples contained lipid components typical of marine sediments, with profiles varying little between samples at the same depth; however, significant differences in PLFA profiles were found between depths of 0 to 1 cm and 13 to 15 cm, reflecting the presence of a different microbial community. Denaturing gradient gel electrophoresis (DGGE) analysis of amplified bacterial 16S rRNA genes revealed that between samples and across sediment core depths of 1 to 4 cm, the community structure appeared homogenous; however, principal-component analysis of DGGE patterns revealed that at greater sediment depths, successional shifts in community structure were evident. Sequencing of DGGE bands and rRNA probe hybridization analysis revealed that the major community members belonged to delta proteobacteria, putative sulfide oxidizers of the gamma proteobacteria, Flavobacteria, Planctomycetales, and Archaea. rRNA hybridization analyses also indicated that these groups were present at similar levels in the top layer across the shelf region.

An integrative study of a meromictic lake ecosystem in Antarctica

In nature, the complexity and structure of microbial communities varies widely, ranging from a few species to thousands of species, and from highly structured to highly unstructured communities. Here, we describe the identity and functional capacity of microbial populations within distinct layers of a pristine, marine-derived, meromictic (stratified) lake (Ace Lake) in Antarctica. Nine million open reading frames were analyzed, representing microbial samples taken from six depths of the lake size fractionated on sequential 3.0, 0.8 and 0.1 μm filters, and including metaproteome data from matching 0.1 μm filters. We determine how the interactions of members of this highly structured and moderately complex community define the biogeochemical fluxes throughout the entire lake. Our view is that the health of this delicate ecosystem is dictated by the effects of the polar light cycle on the dominant role of green sulfur bacteria in primary production and nutrient cycling, and the influence of viruses/phage and phage resistance on the cooperation between members of the microbial community right throughout the lake. To test our assertions, and develop a framework applicable to other microbially driven ecosystems, we developed a mathematical model that describes how cooperation within a microbial system is impacted by periodic fluctuations in environmental parameters on key populations of microorganisms. Our study reveals a mutualistic structure within the microbial community throughout the lake that has arisen as the result of mechanistic interactions between the physico-chemical parameters and the selection of individual members of the community. By exhaustively describing and modelling interactions in Ace Lake, we have developed an approach that may be applicable to learning how environmental perturbations affect the microbial dynamics in more complex aquatic systems.

Chemical characterization of exopolysaccharides from antarctic marine bacteria

Exopolysaccharides (EPS) may have an important role in the Antarctic marine environment, possibly acting as ligands for trace metal nutrients such as iron or providing cryoprotection for growth at low temperature and high salinity. Ten bacterial strains, isolated from Southern Ocean particulate material or from sea ice, were characterized. Whole cell fatty acid profiles and 16S rRNA gene sequences showed that the isolates included representatives of the genera Pseudoalteromonas, Shewanella, Polaribacter, and Flavobacterium as well as one strain, which constituted a new bacterial genus in the family Flavobacteriaceae. The isolates are, therefore, members of the “Gammaproteobacteria” and Cytophaga-Flexibacter-Bacteroides, the taxonomic groups that have been shown to dominate polar sea ice and seawater microbial communities. Exopolysaccharides produced by Antarctic isolates were characterized. Chemical composition and molecular weight data revealed that these EPS were very diverse, even among six closely related Pseudoalteromonas isolates. Most of the EPS contained charged uronic acid residues; several also contained sulfate groups. Some strain produced unusually large polymers (molecular weight up to 5.7 MDa) including one strain in which EPS synthesis is stimulated by low temperature. This study represents a first step in the understanding of the role of bacterial EPS in the Antarctic marine environment.

Annual cycle of fCO2 under sea-ice and in open water in Prydz Bay, East Antarctica

The annual cycle of dissolved nutrients and the fugacity of CO2 (fCO2), calculated from the concentration of dissolved inorganic carbon (DIC) and pH, was studied over a 14-month long period (December 1993 to February 1995) at a site in Prydz Bay near Davis Station, Vestfold Hills, East Antarctica. Significant spring decreases in fCO2 began under the sea-ice in mid-October, when both water column and sea-ice algal activity resulted in the removal of nutrients and DIC and increased pH. Minimum fCO2 (<100 μatm) and lowest nutrient and DIC concentrations occurred in December and January. The low summer fCO2 values were clearly the result of biological activity. The seasonal depletion of dissolved nitrate reached 85% in mid-summer when chlorophyll-a concentrations exceeded 15 mg m−3. Oceanic uptake of carbon dioxide from the atmosphere, calculated from the fugacity difference and daily wind speeds, averaged more than 30 mmol m−2 day−1 during the summer ice-free period. This exchange replaced approximately half of the DIC consumed by biological activity. Apparent nutrient utilisation ratios (C/N/P) were close to Redfield values. In autumn fCO2 began to rise, continuing slowly well into winter, and reaching a maximum close to modern atmospheric values between July and September. This increase can be attributed to a combination of local remineralisation of organic carbon in the water column and the steady increase in the mixing depth of the water column. At first glance, this suggests that air–sea equilibration occurred in winter despite the sea-ice cover, perhaps by horizontal circulation from regions outside the pack ice, or through openings in the ice. However, the persistent 15 to 20% undersaturation of dissolved oxygen throughout the winter suggests an alternate explanation. The late winter fCO2 level may represent a characteristic established by global circulation, so that as a result of increasing atmospheric CO2 concentrations, these Antarctic waters are in transition from being a winter-time source of CO2 to the atmosphere to becoming a sink. Our fCO2 observations emphasize the need to address seasonal variations in assessing Antarctic contributions to the oceanic control of atmospheric CO2.

Ice Shelf Microbial Ecosystems in the High Arctic and Implications for Life on Snowball Earth

Abstract The Ward Hunt Ice Shelf (83°N, 74°W) is the largest remaining section of thick (>10 m) landfast sea ice along the northern coastline of Ellesmere Island, Canada. Extensive meltwater lakes and streams occur on the surface of the ice and are colonized by photosynthetic microbial mat communities. This High Arctic cryo-ecosystem is similar in several of its physical, biological and geochemical features to the McMurdo Ice Shelf in Antarctica. The ice-mats in both polar regions are dominated by filamentous cyanobacteria but also contain diatoms, chlorophytes, flagellates, ciliates, nematodes, tardigrades and rotifers. The luxuriant Ward Hunt consortia also contain high concentrations (107–108 cm–2) of viruses and heterotrophic bacteria. During periods of extensive ice cover, such as glaciations during the Proterozoic, cryotolerant mats of the type now found in these polar ice shelf ecosystems would have provided refugia for the survival, growth and evolution of a variety of organisms, including multicellular eukaryotes.

Metaproteogenomic analysis of a dominant green sulfur bacterium from Ace Lake, Antarctica.

Green sulfur bacteria (GSB) (Chlorobiaceae) are primary producers that are important in global carbon and sulfur cycling in natural environments. An almost complete genome sequence for a single, dominant GSB species (‘C-Ace’) was assembled from shotgun sequence data of an environmental sample taken from the O2–H2S interface of the water column of Ace Lake, Antarctica. Approximately 34 Mb of DNA sequence data were assembled into nine scaffolds totaling 1.79 Mb, representing approximately 19-fold coverage for the C-Ace composite genome. A high level (∼31%) of metaproteomic coverage was achieved using matched biomass. The metaproteogenomic approach provided unique insight into the protein complement required for dominating the microbial community under cold, nutrient-limited, oxygen-limited and extremely varied annual light conditions. C-Ace shows physiological traits that promote its ability to compete very effectively with other GSB and gain dominance (for example, specific bacteriochlorophylls, mechanisms of cold adaptation) as well as a syntrophic relationship with sulfate-reducing bacteria that provides a mechanism for the exchange of sulfur compounds. As a result we are able to propose an explanation of the active biological processes promoted by cold-adapted GSB and the adaptive strategies they use to thrive under the severe physiochemical conditions prevailing in polar environments.

Ice-shelf collapse, climate change, and habitat loss in the Canadian high Arctic

Early explorers in the Canadian high Arctic described a fringe of thick, landfast ice along the 500-km northern coast of Ellesmere Island. This article shows from analyses of historical records, aerial photographs, and satellite imagery (ERS-1, SPOT, RADARSAT-1) that this ancient ice feature (‘Ellesmere Ice Shelf’) underwent a 90% reduction in area during the course of the twentieth century. In addition, hydrographic profiles in Disraeli Fiord (83°N, 74°W) suggest that the ice-shelf remnant that presently dams the fiord (Ward Hunt Ice Shelf) decreased in thickness by 13 m (27%) from 1967 to 1999. Mean annual air temperatures at nearby Alert station showed a significant warming trend during the last two decades of this period, and a significant decline in the number of freezing degree days per annum. The ice-dammed fiord provides a stratified physical and biological environment (epishelf lake) of a type that is otherwise restricted to Antarctica. Extensive meltwater lakes occur on the surface of the ice shelf and support a unique microbial food web. The major contraction of these ice–water habitats foreshadows a much broader loss of marine cryo-ecosystems that will accompany future wanning in the high Arctic.