scholarly journals The Light Responses of Proteorhodopsin-bearing, Antarctic Sea-ice Bacteria

2021 ◽  
Author(s):  
◽  
David Joll Burr

<p>Although homogenous in appearance, Antarctic sea ice forms a complex habitat that is characterised by steep vertical gradients of temperature, irradiance and salinity. Despite these harsh and variable environmental conditions, numerous microbial organisms prosper within Antarctic sea ice. In 2010, bacteria bearing the proteorhodopsin (PR) gene were found within Antarctic sea ice. PR is a photoactive membrane protein that functions as a light-driven proton pump. The hydrogen ion membrane gradient that PR establishes has the potential to drive ATP synthesis, thus allowing PR-bearing bacteria to obtain energy from solar radiation. Although this gene is present in up to 80% of marine bacteria, the active contribution of PR in vivo is debatable. Light induced growth or enhanced survival is generally observed only when PR-bearing bacteria are grown under sub-optimum conditions, such as limited nutrients or carbon, or variations in salinity. This has lead to the general hypothesis that PR has multiple functions, becoming most influential under conditions of stress. In this way, Antarctic sea-ice bacteria may utilise PR to promote survival and enhance energy inputs, when exposed to the harsh conditions of this environment.  To explore this hypothesis, potential PR-bearing isolates were cultured from samples of Antarctic sea-ice bacteria. Using 16S rRNA gene sequencing as well as a comparison of phenotypic and environmental characteristics, the isolates were identified as; Psychrobacter nivimaris, Polaribacter dokdonensis, Paracoccus marcusii and Micrococcus sp. These species, along with Psychroflexus torquis (an Antarctic sea-ice bacterium known to possess PR) were examined for the presence of the PR gene. This gene was identified in P. torquis, Ps. nivimaris and Po. dokdonensis. To my knowledge, this is the first time PR has been found in Ps. nivimaris.  To assess the influence of irradiance on these species, a series of culture based experiments were undertaken. In 2012, a preliminary field experiment was conducted in which a mixed culture of PR-bearing and non PR-bearing bacteria; Ps. nivimaris, Po. dokdonensis, Pa. marcusii and Micrococcus sp., was incubated in situ in the annual sea ice surrounding Ross Island, Antarctica. The method developed for these experiments is unique, in that cultures of sea-ice bacteria have not before been incubated within their natural environment. No major differences in growth patterns were observed when bacteria were incubated under different wavelengths and light intensities, however, valuable insight into methodological improvement was obtained. Using these refinements, a second in situ incubation experiment was conducted at the same field site, in 2013. Over this 2 week incubation, monocultures of P. torquis grown in full strength media grew most readily under 50%- and blue-light treatments, with red- and green-light yielding lower biomasses, and no growth occurring in the dark. Ambient sea-ice irradiance resulted in highly variable growth, attributed to high irradiance growth-inhibition. These results indicate that P. torquis utilises low levels of light in order to increase its growth in Antarctic sea ice.  The influence of light on the growth of P. torquis, Ps. nivimaris and Po. dokdonensis was examined in a laboratory-based experiment, in which media strength and temperature were varied. When cultured at 12°C, Ps. nivimaris grown under constant irradiance reached a higher biomass than in darkness. This trend was most pronounced when this species was cultured in a 10% media concentration. A trend of decreased exponential-growth was observed in light-incubated cultures of Ps. nivimaris, grown at 4°C or -1°C. Elevated maximum growth of Po. dokdonensis was observed under irradiated conditions in the 10% media treatment. This species however, only grew at 12°C; an unexpected result for an Antarctic microbe. P. torquis was not affected by irradiance under any culture conditions and did not grow at -1°C. This last result contrasts the results of the in situ incubations and may have been affected by factors such as culture age.  This research demonstrates multiple examples of light-enhanced growth occurring in PR-bearing Antarctic sea-ice bacteria, with the most prominent trends occurring in reduced concentration media. Therefore, this work agrees with the overarching hypothesis that PR is most influential under conditions of stress. The varying effect of temperature on the influence of PR suggests that some species are able to use this protein at low temperatures, whilst others cannot. Therefore, PR likely provides a selective advantage to some species, depending on a variety of physicochemical factors, including nutrient and carbon availability, salinity and temperature.</p>

2021 ◽  
Author(s):  
◽  
David Joll Burr

<p>Although homogenous in appearance, Antarctic sea ice forms a complex habitat that is characterised by steep vertical gradients of temperature, irradiance and salinity. Despite these harsh and variable environmental conditions, numerous microbial organisms prosper within Antarctic sea ice. In 2010, bacteria bearing the proteorhodopsin (PR) gene were found within Antarctic sea ice. PR is a photoactive membrane protein that functions as a light-driven proton pump. The hydrogen ion membrane gradient that PR establishes has the potential to drive ATP synthesis, thus allowing PR-bearing bacteria to obtain energy from solar radiation. Although this gene is present in up to 80% of marine bacteria, the active contribution of PR in vivo is debatable. Light induced growth or enhanced survival is generally observed only when PR-bearing bacteria are grown under sub-optimum conditions, such as limited nutrients or carbon, or variations in salinity. This has lead to the general hypothesis that PR has multiple functions, becoming most influential under conditions of stress. In this way, Antarctic sea-ice bacteria may utilise PR to promote survival and enhance energy inputs, when exposed to the harsh conditions of this environment.  To explore this hypothesis, potential PR-bearing isolates were cultured from samples of Antarctic sea-ice bacteria. Using 16S rRNA gene sequencing as well as a comparison of phenotypic and environmental characteristics, the isolates were identified as; Psychrobacter nivimaris, Polaribacter dokdonensis, Paracoccus marcusii and Micrococcus sp. These species, along with Psychroflexus torquis (an Antarctic sea-ice bacterium known to possess PR) were examined for the presence of the PR gene. This gene was identified in P. torquis, Ps. nivimaris and Po. dokdonensis. To my knowledge, this is the first time PR has been found in Ps. nivimaris.  To assess the influence of irradiance on these species, a series of culture based experiments were undertaken. In 2012, a preliminary field experiment was conducted in which a mixed culture of PR-bearing and non PR-bearing bacteria; Ps. nivimaris, Po. dokdonensis, Pa. marcusii and Micrococcus sp., was incubated in situ in the annual sea ice surrounding Ross Island, Antarctica. The method developed for these experiments is unique, in that cultures of sea-ice bacteria have not before been incubated within their natural environment. No major differences in growth patterns were observed when bacteria were incubated under different wavelengths and light intensities, however, valuable insight into methodological improvement was obtained. Using these refinements, a second in situ incubation experiment was conducted at the same field site, in 2013. Over this 2 week incubation, monocultures of P. torquis grown in full strength media grew most readily under 50%- and blue-light treatments, with red- and green-light yielding lower biomasses, and no growth occurring in the dark. Ambient sea-ice irradiance resulted in highly variable growth, attributed to high irradiance growth-inhibition. These results indicate that P. torquis utilises low levels of light in order to increase its growth in Antarctic sea ice.  The influence of light on the growth of P. torquis, Ps. nivimaris and Po. dokdonensis was examined in a laboratory-based experiment, in which media strength and temperature were varied. When cultured at 12°C, Ps. nivimaris grown under constant irradiance reached a higher biomass than in darkness. This trend was most pronounced when this species was cultured in a 10% media concentration. A trend of decreased exponential-growth was observed in light-incubated cultures of Ps. nivimaris, grown at 4°C or -1°C. Elevated maximum growth of Po. dokdonensis was observed under irradiated conditions in the 10% media treatment. This species however, only grew at 12°C; an unexpected result for an Antarctic microbe. P. torquis was not affected by irradiance under any culture conditions and did not grow at -1°C. This last result contrasts the results of the in situ incubations and may have been affected by factors such as culture age.  This research demonstrates multiple examples of light-enhanced growth occurring in PR-bearing Antarctic sea-ice bacteria, with the most prominent trends occurring in reduced concentration media. Therefore, this work agrees with the overarching hypothesis that PR is most influential under conditions of stress. The varying effect of temperature on the influence of PR suggests that some species are able to use this protein at low temperatures, whilst others cannot. Therefore, PR likely provides a selective advantage to some species, depending on a variety of physicochemical factors, including nutrient and carbon availability, salinity and temperature.</p>


mSystems ◽  
2021 ◽  
Vol 6 (2) ◽  
Author(s):  
Daphne K. Welter ◽  
Albane Ruaud ◽  
Zachariah M. Henseler ◽  
Hannah N. De Jong ◽  
Peter van Coeverden de Groot ◽  
...  

ABSTRACT Host-adapted microorganisms are generally assumed to have evolved from free-living, environmental microorganisms, as examples of the reverse process are rare. In the phylum Gammaproteobacteria, family Moraxellaceae, the genus Psychrobacter includes strains from a broad ecological distribution including animal bodies as well as sea ice and other nonhost environments. To elucidate the relationship between these ecological niches and Psychrobacter’s evolutionary history, we performed tandem genomic analyses with phenotyping of 85 Psychrobacter accessions. Phylogenomic analysis of the family Moraxellaceae reveals that basal members of the Psychrobacter clade are Moraxella spp., a group of often-pathogenic organisms. Psychrobacter exhibited two broad growth patterns in our phenotypic screen: one group that we called the “flexible ecotype” (FE) had the ability to grow between 4 and 37°C, and the other, which we called the “restricted ecotype” (RE), could grow between 4 and 25°C. The FE group includes phylogenetically basal strains, and FE strains exhibit increased transposon copy numbers, smaller genomes, and a higher likelihood to be bile salt resistant. The RE group contains only phylogenetically derived strains and has increased proportions of lipid metabolism and biofilm formation genes, functions that are adaptive to cold stress. In a 16S rRNA gene survey of polar bear fecal samples, we detect both FE and RE strains, but in in vivo colonizations of gnotobiotic mice, only FE strains persist. Our results indicate the ability to grow at 37°C, seemingly necessary for mammalian gut colonization, is an ancestral trait for Psychrobacter, which likely evolved from a pathobiont. IMPORTANCE Host-associated microbes are generally assumed to have evolved from free-living ones. The evolutionary transition of microbes in the opposite direction, from host associated toward free living, has been predicted based on phylogenetic data but not studied in depth. Here, we provide evidence that the genus Psychrobacter, particularly well known for inhabiting low-temperature, high-salt environments such as sea ice, permafrost soils, and frozen foodstuffs, has evolved from a mammalian-associated ancestor. We show that some Psychrobacter strains retain seemingly ancestral genomic and phenotypic traits that correspond with host association while others have diverged to psychrotrophic or psychrophilic lifestyles.


2011 ◽  
Vol 23 (4) ◽  
pp. 399-409 ◽  
Author(s):  
Gregory H. Leonard ◽  
Patricia J. Langhorne ◽  
Michael J.M. Williams ◽  
Ross Vennell ◽  
Craig R. Purdie ◽  
...  

AbstractHere we describe the evolution through winter of a layer of in situ supercooled water beneath the sea ice at a site close to the McMurdo Ice Shelf. From early winter (May), the temperature of the upper water column was below its surface freezing point, implying contact with an ice shelf at depth. By late winter the supercooled layer was c. 40 m deep with a maximum supercooling of c. 25 mK located 1–2 m below the sea ice-water interface. Transitory in situ supercooling events were also observed, one lasting c. 17 hours and reaching a depth of 70 m. In spite of these very low temperatures the isotopic composition of the water was relatively heavy, suggesting little glacial melt. Further, the water's temperature-salinity signature indicates contributions to water mass properties from High Salinity Shelf Water produced in areas of high sea ice production to the north of McMurdo Sound. Our measurements imply the existence of a heat sink beneath the supercooled layer that extracts heat from the ocean to thicken and cool this layer and contributes to the thickness of the sea ice cover. This sink is linked to the circulation pattern of the McMurdo Sound.


2015 ◽  
Vol 9 (11) ◽  
pp. 2537-2540 ◽  
Author(s):  
Christiane Uhlig ◽  
Fabian Kilpert ◽  
Stephan Frickenhaus ◽  
Jessica U Kegel ◽  
Andreas Krell ◽  
...  

2018 ◽  
Author(s):  
Daniel Price ◽  
Iman Soltanzadeh ◽  
Wolfgang Rack

Abstract. Knowledge of the snow depth distribution on Antarctic sea ice is poor but is critical to obtaining sea ice thickness from satellite altimetry measurements of freeboard. We examine the usefulness of various snow products to provide snow depth information over Antarctic fast ice with a focus on a novel approach using a high-resolution numerical snow accumulation model (SnowModel). We compare this model to results from ECMWF ERA-Interim precipitation, EOS Aqua AMSR-E passive microwave snow depths and in situ measurements at the end of the sea ice growth season. The fast ice was segmented into three areas by fastening date and the onset of snow accumulation was calibrated to these dates. SnowModel falls within 0.02 m snow water equivalent (swe) of in situ measurements across the entire study area, but exhibits deviations of 0.05 m swe from these measurements in the east where large topographic features appear to have caused a positive bias in snow depth. AMSR-E provides swe values half that of SnowModel for the majority of the sea ice growth season. The coarser resolution ERA-Interim, not segmented for sea ice freeze up area reveals a mean swe value 0.01 m higher than in situ measurements. These various snow datasets and in situ information are used to infer sea ice thickness in combination with CryoSat-2 (CS-2) freeboard data. CS-2 is capable of capturing the seasonal trend of sea ice freeboard growth but thickness results are highly dependent on the assumptions involved in separating snow and ice freeboard. With various assumptions about the radar penetration into the snow cover, the sea ice thickness estimates vary by up to 2 m. However, we find the best agreement between CS-2 derived and in situ thickness when a radar penetration of 0.05-0.10 m into the snow cover is assumed.


Elem Sci Anth ◽  
2021 ◽  
Vol 9 (1) ◽  
Author(s):  
Caroline Jacques ◽  
Célia J. Sapart ◽  
François Fripiat ◽  
Gauthier Carnat ◽  
Jiayun Zhou ◽  
...  

We report on methane (CH4) stable isotope (δ13C and δ2H) measurements from landfast sea ice collected near Barrow (Utqiagvik, Alaska) and Cape Evans (Antarctica) over the winter-to-spring transition. These measurements provide novel insights into pathways of CH4 production and consumption in sea ice. We found substantial differences between the two sites. Sea ice overlying the shallow shelf of Barrow was supersaturated in CH4 with a clear microbial origin, most likely from methanogenesis in the sediments. We estimated that in situ CH4 oxidation consumed a substantial fraction of the CH4 being supplied to the sea ice, partly explaining the large range of isotopic values observed (δ13C between –68.5 and –48.5 ‰ and δ2H between –246 and –104 ‰). Sea ice at Cape Evans was also supersaturated in CH4 but with surprisingly high δ13C values (between –46.9 and –13.0 ‰), whereas δ2H values (between –313 and –113 ‰) were in the range of those observed at Barrow. These are the first measurements of CH4 isotopic composition in Antarctic sea ice. Our data set suggests a potential combination of a hydrothermal source, in the vicinity of the Mount Erebus, with aerobic CH4 formation in sea ice, although the metabolic pathway for the latter still needs to be elucidated. Our observations show that sea ice needs to be considered as an active biogeochemical interface, contributing to CH4 production and consumption, which disputes the standing paradigm that sea ice is an inert barrier passively accumulating CH4 at the ocean-atmosphere boundary.


2011 ◽  
Vol 23 (6) ◽  
pp. 531-536 ◽  
Author(s):  
Rebecca O.M. Cowie ◽  
Elizabeth W. Maas ◽  
Ken G. Ryan

AbstractArchaea, once thought to be only extremophiles, are now known to be abundant in most environments. They can predominate in microbial communities and be significantly involved in many global biogeochemical cycles. However, Archaea have not been reported in Antarctic sea ice. Our understanding of the ecology of Antarctic sea ice prokaryotes is still in its infancy but this information is important if we are to understand their diversity, adaptations and biogeochemical roles in Antarctic systems. We detected Archaea in sea ice at two sampling sites taken from three subsequent years using conserved 16S rRNA gene archaeal primers and PCR. Archaeal abundance was measured using quantitative PCR and community diversity was investigated by sequencing cloned 16S rRNA gene PCR products. Archaea in Antarctic sea ice were found to be in low abundance consisting of ≤ 6.6% of the prokaryotic community. The majority, 90.8% of the sequences, clustered with the recently described phylumThaumarchaeota, one group closely clustered with the ammonia-oxidizing CandidatusNitrosopumilus maritimus. The remainder of the clones grouped with theEuryarchaeota.


2019 ◽  
Vol 13 (4) ◽  
pp. 1409-1422
Author(s):  
Daniel Price ◽  
Iman Soltanzadeh ◽  
Wolfgang Rack ◽  
Ethan Dale

Abstract. Knowledge of the snow depth distribution on Antarctic sea ice is poor but is critical to obtaining sea ice thickness from satellite altimetry measurements of the freeboard. We examine the usefulness of various snow products to provide snow depth information over Antarctic fast ice in McMurdo Sound with a focus on a novel approach using a high-resolution numerical snow accumulation model (SnowModel). We compare this model to results from ECMWF ERA-Interim precipitation, EOS Aqua AMSR-E passive microwave snow depths and in situ measurements at the end of the sea ice growth season in 2011. The fast ice was segmented into three areas by fastening date and the onset of snow accumulation was calibrated to these dates. SnowModel captures the spatial snow distribution gradient in McMurdo Sound and falls within 2 cm snow water equivalent (s.w.e) of in situ measurements across the entire study area. However, it exhibits deviations of 5 cm s.w.e. from these measurements in the east where the effect of local topographic features has caused an overestimate of snow depth in the model. AMSR-E provides s.w.e. values half that of SnowModel for the majority of the sea ice growth season. The coarser-resolution ERA-Interim produces a very high mean s.w.e. value 20 cm higher than the in situ measurements. These various snow datasets and in situ information are used to infer sea ice thickness in combination with CryoSat-2 (CS-2) freeboard data. CS-2 is capable of capturing the seasonal trend of sea ice freeboard growth but thickness results are highly dependent on what interface the retracked CS-2 height is assumed to represent. Because of this ambiguity we vary the proportion of ice and snow that represents the freeboard – a mathematical alteration of the radar penetration into the snow cover – and assess this uncertainty in McMurdo Sound. The ranges in sea ice thickness uncertainty within these bounds, as means of the entire growth season, are 1.08, 4.94 and 1.03 m for SnowModel, ERA-Interim and AMSR-E respectively. Using an interpolated in situ snow dataset we find the best agreement between CS-2-derived and in situ thickness when this interface is assumed to be 0.07 m below the snow surface.


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