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Discipline
Biological
Keywords
Gas-Floating Aggregates
Antarctica
Observation Type
Standalone
Nature
Orphan Data
Submitted
Feb 3rd, 2017
Published
Dec 12th, 2017
  • Abstract

    We report the formation of gas-vesicle stalked aggregates formed by a mucoid-sediment layer colonized by pennate diatoms and occasional centric diatoms. The most frequently occurring diatoms within this layer belonged to Pleurosigma sp., with less abundance in the stalk. Aggregates stayed attached to the sediment up to ten days until the buoyant force was sufficient to release them from the bottom. The structures were observed twice, in outdoor tanks (250 L) containing marine sediments in filtered seawater under natural light cycle and ambient temperature (-1.3 to 0.6 ºC), after 15 days. Whether this mechanism occurs in the field awaits elucidation. However, it stands out as a pathway for benthic diatom dispersion, resuspension and benthic-pelagic coupling for Antarctic coastal systems.

  • Figure
  • Introduction

    Benthic microbial mats are a common feature in Antarctic lake beds and are primarily comprised of cyanobacteria associated with pennate diatoms. They contribute to the biostabilization of soft bottoms and can be the most abundant and productive ecosystems in continental Antarctica. Several morphotypes are recognised, including some floating types. Fewer references are available for marine systems, such as intertidal sandy 'sediment rafting', where diatom extracellular mucopolysaccharides dry out during low tide, peel off the substratum and float onto the water surface carrying sand grains together. The importance of floating diatoms associations is recognized since they are involved in the dispersion of species or communities, but also in the removal and transport of organic and inorganic matter. In addition, they may play a major role in the benthic-pelagic coupling, contributing to the energy and matter flow, and nutrient cycling.

  • Objective

    Report of the development and release of gas-filled-aggregates of benthic diatoms on Antarctic marine sediments.

  • Results & Discussion

    The development and release of gas-filled, aggregates formed by diatoms immersed in a marine mucoid-sediment layer were observed. They consisted of a gas-filled aggregate stalked structure (5.4–5.6 mm in diameter and 1–3 cm height including the stalk) (Fig. 1A, 1B). The microscopic assessment of collected aggregates, allowed us to identify a mucoid-sediment layer colonized by living diatoms (Fig. 1C) and the occurrence of bacteria.

    The structures were composed mainly of pennate diatoms with occasional centric diatoms. A general lower abundance of diatoms was observed in the stalk compared to the gas-filled part (Fig. 1D). The most frequently occurring and by far dominant genus within the layer belonged to Pleurosigma sp. (Fig. 1C, 1D). Other occurring pennate taxa were Achnanthes, Amphora, Cocconeis, Fragilaria, Gyrosigma, Licmophora, Nitzschia and naviculoids.

    Aggregates stayed attached to the sediments by their elongated stalks for up to 10 days until the buoyant force was sufficient to release them from the bottom. We were not able to characterize the gas entrapped in the head of the structure, nor the origin of it. We assume that buoyancy was caused by the accumulation of photosynthetically produced gases (probably oxygen) according with,,.

    In coincidence with and, these structures developed and released in stable bed sediments, in the absence of currents and under a presumably high light intensity. Our system was characterized also by the absence of mesograzers. High light intensity after sea ice melting in early summer or resuspension of bottom sediment have been ascribed as main drivers of increased abundances of benthic diatoms in Antarctic nearshore waters. We recognized these three as potential drivers of our finding. Light intensity seems to be a key factor involved in the occurrence of stalked gas-aggregates formation. Photosynthetically active radiation (PAR) in Potter Cove during summer can be 734 (+291) µmol m-2 s-1 below the surface (10 cm) which is much higher than 0.4 to 1.2 µmol m-2 s-1 reported by. While such high radiation may have a potentially detrimental effect, Antarctic marine benthic diatoms are highly resistant to UV radiation. Sediments were artificially resuspended in the tanks and were let to settle in stable bed sediments exposed to high radiation. Resuspension may be relevant before stabilization of the sediment bed, by making nutrients confined in sediments available for diatom growth. As the tanks were set outdoor and there were snowfall and light rain in some days, we assume that some change in salinity may have occurred. However, we dismiss any potential negative effect on diatoms, since low salinity (even artificially extreme values) on marine pennate benthic diatoms has no evident effect on growth or photosynthetic activity.

  • Conclusions

    Floating aggregates of diatoms have been described in the Arctic, occurring underneath sea ice and in melt ponds, related to high light radiance, low salinity and nutrients depletion. Recently, a massive growth of benthic diatoms was reported in a close location that has also experienced glacier retreat (Marian Cove, South Shetland Islands), however, the development of stalked gas-aggregates was not described.

    To our knowledge, the occurrence of benthic microalgal aggregations and their detachment by buoyancy have been only described for freshwater systems. Thus, we are not aware of a similar process for marine coastal soft bottom benthos in Antarctica and, therefore, our observation signal the potential of its occurrence in the field. If this finding was confirmed, it would be of great relevance by promoting a vertical flow of energy and matter and nutrient replenishment in the water column, as proved in freshwater ecosystems. Besides, this mechanism stands out for a potential relevance for benthic diatoms dispersion and its implications as an entry pathway to the water column and bentho-pelagic coupling.

    Finally, although these observations were made under artificial conditions, we signal three potential drivers of the development of these structures: 1) the resuspension and stabilization of sediments, 2) lower salinity and 3) high PAR irradiance.

  • Limitations

    This short note describes the formation and release of stalked gas-filled, diatom aggregates developed on marine sediments in Antarctica, and presents two main limitations: 1) the aggregates occurred under artificial conditions (outdoor, 250 L tanks), with absence of mesograzers; 2) the lack of monitoring of salinity, temperature, nutrients and light. In particular, salinity may have been altered due to evaporation, snowfall and rain.

  • Methods

    Sediment samples were collected in the inner part of Potter Cove (South Shetland Islands, Antarctica) by means of a Van Veen grab at Station I at 12 m depth, during the Austral summer 2013-2014. Following, the sediment was sieved through decreasing mesh sizes (final sieve: 50 μm) to remove infaunal organisms, detritus, gravel and fine sand. The clay and fine silt fractions were removed by resuspension in filtered sea water (0.5 μm) and elimination of the supernatant after 5 min of sedimentation. Finally, it was re-suspended again and let to settle for 48 h to be used for a further experiment. The remaining sediments were kept in filtered seawater under natural light cycle and ambient temperature (-1.3 to 0.6 ºC) in outdoor tanks (250 L). After 2 weeks, we noticed the occurrence of the reported stalked aggregates. We performed the same procedure twice, and, in both cases, the same phenomenon was observed. On the second occasion, aggregates were photographed in situ (submersible digital camera Panasonic Lumix dmc-ts25). Twenty four vesicles were carefully detached and collected individually in filtered seawater (February 22nd, 2014). A subset was observed with an Olympus SZX-7 stereomicroscope equipped with an Olympus DP21 digital camera. Slides of the stalk and head were observed with an Olympus BX53F light microscope equipped with an Olympus DP21 digital camera to account for the general taxonomic composition. Finally, permanent slides of cleaned material of a subset of lugol-fixed samples were prepared using Naphrax. Pictures were taken using a phase contrast Leica DM 2500 light microscope equipped with a Leica DFC420 digital camera.

  • Acknowledgements

    We thank the support of Instituto Antártico Argentino-Dirección Nacional del Antártico, Carlini Station and Dallmann Laboratory crews. We are very grateful to Dr. Cefarelli and Dr. Ferrario for the help in the identification, Dr. A. Wulff for helpful suggestions, Dr. M.L. Quartino (IAA-DNA) and two anonymous reviewers that have substantially improved this work. It was supported by grants from DNA-IAA (PICTA 7/2008-2011), ANPCyT-DNA (PICTO 0116/2012-2015) INST18H (IAA-DNA), CONICET (Doctoral Fellowship), Total Foundation (ECLIPSE Project) and IMCONet Program (Marie Curie Action IRSES Action No. 318718).

  • Ethics statement

    Not Applicable.

  • References
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    Matters Select15.5/20

    Gas-floating aggregates of Antarctic benthic diatoms

    Affiliation listing not available.
    Abstractlink

    We report the formation of gas-vesicle stalked aggregates formed by a mucoid-sediment layer colonized by pennate diatoms and occasional centric diatoms. The most frequently occurring diatoms within this layer belonged to Pleurosigma sp., with less abundance in the stalk. Aggregates stayed attached to the sediment up to ten days until the buoyant force was sufficient to release them from the bottom. The structures were observed twice, in outdoor tanks (250 L) containing marine sediments in filtered seawater under natural light cycle and ambient temperature (-1.3 to 0.6 ºC), after 15 days. Whether this mechanism occurs in the field awaits elucidation. However, it stands out as a pathway for benthic diatom dispersion, resuspension and benthic-pelagic coupling for Antarctic coastal systems.

    Figurelink

    Figure 1. Gas-vesicle aggregates of benthic diatoms.

    (A) In situ picture of the benthic diatoms aggregates attached to the bottom of the outdoor tank.

    (B) Closer view of a recently released aggregate kept in filtered seawater.

    (C) Mucoid layer of the aggregates.

    (D) Diatoms occurring in the aggregate; note the dominance of Pleurosigma sp.

    Introductionlink

    Benthic microbial mats are a common feature in Antarctic lake beds and are primarily comprised of cyanobacteria associated with pennate diatoms[1]. They contribute to the biostabilization of soft bottoms and can be the most abundant and productive ecosystems in continental Antarctica[2]. Several morphotypes are recognised, including some floating types[1][3][4]. Fewer references are available for marine systems, such as intertidal sandy 'sediment rafting', where diatom extracellular mucopolysaccharides dry out during low tide, peel off the substratum and float onto the water surface carrying sand grains together[5]. The importance of floating diatoms associations is recognized since they are involved in the dispersion of species or communities, but also in the removal and transport of organic and inorganic matter[6]. In addition, they may play a major role in the benthic-pelagic coupling, contributing to the energy and matter flow, and nutrient cycling[4].

    Objectivelink

    Report of the development and release of gas-filled-aggregates of benthic diatoms on Antarctic marine sediments.

    Results & Discussionlink

    The development and release of gas-filled, aggregates formed by diatoms immersed in a marine mucoid-sediment layer were observed. They consisted of a gas-filled aggregate stalked structure (5.4–5.6 mm in diameter and 1–3 cm height including the stalk) (Fig. 1A, 1B). The microscopic assessment of collected aggregates, allowed us to identify a mucoid-sediment layer colonized by living diatoms (Fig. 1C) and the occurrence of bacteria.

    The structures were composed mainly of pennate diatoms with occasional centric diatoms. A general lower abundance of diatoms was observed in the stalk compared to the gas-filled part (Fig. 1D). The most frequently occurring and by far dominant genus within the layer belonged to Pleurosigma sp. (Fig. 1C, 1D). Other occurring pennate taxa were Achnanthes, Amphora, Cocconeis, Fragilaria, Gyrosigma, Licmophora, Nitzschia and naviculoids.

    Aggregates stayed attached to the sediments by their elongated stalks for up to 10 days until the buoyant force was sufficient to release them from the bottom. We were not able to characterize the gas entrapped in the head of the structure, nor the origin of it. We assume that buoyancy was caused by the accumulation of photosynthetically produced gases (probably oxygen) according with[1],[7],[8].

    In coincidence with[9] and[6], these structures developed and released in stable bed sediments, in the absence of currents and under a presumably high light intensity. Our system was characterized also by the absence of mesograzers. High light intensity after sea ice melting in early summer or resuspension of bottom sediment have been ascribed as main drivers of increased abundances of benthic diatoms in Antarctic nearshore waters[10][11][12]. We recognized these three as potential drivers of our finding. Light intensity seems to be a key factor involved in the occurrence of stalked gas-aggregates formation[1][6]. Photosynthetically active radiation (PAR) in Potter Cove during summer can be 734 (+291) µmol m-2 s-1[13] below the surface (10 cm) which is much higher than 0.4 to 1.2 µmol m-2 s-1 reported by[1]. While such high radiation may have a potentially detrimental effect, Antarctic marine benthic diatoms are highly resistant to UV radiation[14]. Sediments were artificially resuspended in the tanks and were let to settle in stable bed sediments exposed to high radiation. Resuspension may be relevant before stabilization of the sediment bed, by making nutrients confined in sediments available for diatom growth[15]. As the tanks were set outdoor and there were snowfall and light rain in some days, we assume that some change in salinity may have occurred. However, we dismiss any potential negative effect on diatoms, since low salinity (even artificially extreme values) on marine pennate benthic diatoms has no evident effect on growth or photosynthetic activity[16].

    Conclusionslink

    Floating aggregates of diatoms have been described in the Arctic, occurring underneath sea ice and in melt ponds, related to high light radiance, low salinity and nutrients depletion[7][8]. Recently, a massive growth of benthic diatoms was reported in a close location that has also experienced glacier retreat (Marian Cove, South Shetland Islands)[17], however, the development of stalked gas-aggregates was not described.

    To our knowledge, the occurrence of benthic microalgal aggregations and their detachment by buoyancy have been only described for freshwater systems. Thus, we are not aware of a similar process for marine coastal soft bottom benthos in Antarctica and, therefore, our observation signal the potential of its occurrence in the field. If this finding was confirmed, it would be of great relevance by promoting a vertical flow of energy and matter and nutrient replenishment in the water column, as proved in freshwater ecosystems. Besides, this mechanism stands out for a potential relevance for benthic diatoms dispersion and its implications as an entry pathway to the water column and bentho-pelagic coupling.

    Finally, although these observations were made under artificial conditions, we signal three potential drivers of the development of these structures: 1) the resuspension and stabilization of sediments, 2) lower salinity and 3) high PAR irradiance.

    Limitationslink

    This short note describes the formation and release of stalked gas-filled, diatom aggregates developed on marine sediments in Antarctica, and presents two main limitations: 1) the aggregates occurred under artificial conditions (outdoor, 250 L tanks), with absence of mesograzers; 2) the lack of monitoring of salinity, temperature, nutrients and light. In particular, salinity may have been altered due to evaporation, snowfall and rain.

    Methodslink

    Sediment samples were collected in the inner part of Potter Cove (South Shetland Islands, Antarctica) by means of a Van Veen grab at Station I[18] at 12 m depth, during the Austral summer 2013-2014. Following[19], the sediment was sieved through decreasing mesh sizes (final sieve: 50 μm) to remove infaunal organisms, detritus, gravel and fine sand. The clay and fine silt fractions were removed by resuspension in filtered sea water (0.5 μm) and elimination of the supernatant after 5 min of sedimentation. Finally, it was re-suspended again and let to settle for 48 h to be used for a further experiment. The remaining sediments were kept in filtered seawater under natural light cycle and ambient temperature (-1.3 to 0.6 ºC) in outdoor tanks (250 L). After 2 weeks, we noticed the occurrence of the reported stalked aggregates. We performed the same procedure twice, and, in both cases, the same phenomenon was observed. On the second occasion, aggregates were photographed in situ (submersible digital camera Panasonic Lumix dmc-ts25). Twenty four vesicles were carefully detached and collected individually in filtered seawater (February 22nd, 2014). A subset was observed with an Olympus SZX-7 stereomicroscope equipped with an Olympus DP21 digital camera. Slides of the stalk and head were observed with an Olympus BX53F light microscope equipped with an Olympus DP21 digital camera to account for the general taxonomic composition. Finally, permanent slides of cleaned material of a subset of lugol-fixed samples were prepared using Naphrax[20][21]. Pictures were taken using a phase contrast Leica DM 2500 light microscope equipped with a Leica DFC420 digital camera.

    Acknowledgementslink

    We thank the support of Instituto Antártico Argentino-Dirección Nacional del Antártico, Carlini Station and Dallmann Laboratory crews. We are very grateful to Dr. Cefarelli and Dr. Ferrario for the help in the identification, Dr. A. Wulff for helpful suggestions, Dr. M.L. Quartino (IAA-DNA) and two anonymous reviewers that have substantially improved this work. It was supported by grants from DNA-IAA (PICTA 7/2008-2011), ANPCyT-DNA (PICTO 0116/2012-2015) INST18H (IAA-DNA), CONICET (Doctoral Fellowship), Total Foundation (ECLIPSE Project) and IMCONet Program (Marie Curie Action IRSES Action No. 318718).

    visibility_offConflict of Interest hidden to preserve triple blindness.
    Ethics Statementlink

    Not Applicable.

    No fraudulence is committed in performing these experiments or during processing of the data. We understand that in the case of fraudulence, the study can be retracted by ScienceMatters.

    Referenceslink
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      REMOVAL OF ORGANIC AND INORGANIC MATTER FROM ANTARCTIC LAKES BY AERIAL ESCAPE OF BLUEGREEN ALGAL MATS
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      Salinity, depth and the structure and composition of microbial mats in continental Antarctic lakes
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      Distribution of algal aggregates under summer sea ice in the Central Arctic
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    10. Ahn I.-Y., Chung Hosung, Kang Jae-Shin, Kang Sung-Ho
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      Seasonal variation of microalgal assemblages at a fixed station in King George Island, Antarctica, 1996
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    14. Angela, Wulff, Michael Y., Roleda, Katharina, Zacher, Christian, Wiencke
      UV radiation effects on pigments, photosynthetic efficiency and DNA of an Antarctic marine benthic diatom community
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      Coupled Response of Bacterial Production to a Wind-Induced Fall Phytoplankton Bloom and Sediment Resuspension in the Chukchi Sea Shelf, Western Arctic Ocean
      Frontiers in Marine Science, 3/2016, page 231 DOI: 10.3389/fmars.2016.00231chrome_reader_mode
    16. Wulff, Angela, Torstensson, Anders, Campana, Gabriela Laura,more_horiz, Zacher, Katharina
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    17. Ahn In-Young, Moon Hye-Won, Jeon Misa, Kang Sung-Ho
      First record of massive blooming of benthic diatoms and their association with megabenthic filter feeders on the shallow seafloor of an Antarctic Fjord: Does glacier melting fuel the bloom?
      Ocean Science Journal, 51/2016, pages 273-279 DOI: 10.1007/s12601-016-0023-ychrome_reader_mode
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