Metabolome-mediated biocryomorphic evolution promotes carbon fixation in Greenlandic cryoconite holes
Journal article
Joseph M Cook, Arwyn Edwards, Bulling, M., Luis A J Mur, Sophie Cook, Jarishma K Gokul, Karen A Cameron, Sweet, M. and Tristram D L Irvine-Fynn 2016. Metabolome-mediated biocryomorphic evolution promotes carbon fixation in Greenlandic cryoconite holes. Environmental Microbiology. https://doi.org/10.1111/1462-2920.13349
| Authors | Joseph M Cook, Arwyn Edwards, Bulling, M., Luis A J Mur, Sophie Cook, Jarishma K Gokul, Karen A Cameron, Sweet, M. and Tristram D L Irvine-Fynn |
|---|---|
| Abstract | Microbial photoautotrophs on glaciers engineer the formation of granular microbial-mineral aggregate stermed cryoconite which accelerate ice melt, creating quasi-cylindrical pits called ‘cryoconite holes’. Theseact as biogeochemical reactors on the ice surface and provide habitats for remarkably active and diverse microbiota. Evolution of cryoconite holes towards an equilibrium depth is well known, yet inter-actions between microbial activity and hole morphology are currently weakly addressed. Here, we experimentally perturbed the depths and diameters of cryoconite holes on the Greenland Ice Sheet.Cryoconite holes responded by sensitively adjusting their shapes in three dimensions (‘biocryomorphic evolution’) thus maintaining favourable conditions for net autotrophy at the hole floors. Non-targeted metabolomics reveals concomitant shifts in cyclicAMP and fucose metabolism consistent with photo-taxis and extracellular polymer synthesis indicating metabolomic-level granular changes in response to perturbation. We present a conceptual model explain-ing this process and suggest that it results in remarkably robust net autotrophy on the Greenland Ice Sheet. We also describe observations of cryocon-ite migrating away from shade, implying a degree of self-regulation of carbon budgets over mesoscales. Since cryoconite is a microbe-mineral aggregate, itappears that microbial processes themselves formand maintain stable autotrophic habitats on the sur-face of the Greenland ice sheet. |
| Keywords | greenland; ice sheet; Microbial photoautotrophs |
| Year | 2016 |
| Journal | Environmental Microbiology |
| ISSN | 14622912 |
| Digital Object Identifier (DOI) | https://doi.org/10.1111/1462-2920.13349 |
| Web address (URL) | http://doi.wiley.com/10.1111/1462-2920.13349 |
| http://eprints.whiterose.ac.uk/102375/ | |
| hdl:10545/618779 | |
| Output status | Published |
| Publication dates | 2016 |
| Publication process dates | |
| Deposited | 25 Aug 2016, 10:37 |
| Accepted | 19 Apr 2016 |
| Rights | Archived with thanks to Environmental Microbiology |
| Contributors | University of Derby, Department of Geography; University of Sheffield; Sheffield UK S10 2TN, Institute of Biological, Environmental and Rural Sciences; Aberystwyth University; SY23 3DA, College of Life and Natural Sciences; University of Derby; UK DE22 1GB, Institute of Biological, Environmental and Rural Sciences; Aberystwyth University; SY23 3DA, Institute of Biological, Environmental and Rural Sciences; Aberystwyth University; SY23 3DA, Department of Geochemistry; Geological Survey of Denmark and Greenland (GEUS); 1350 Copenhagen Denmark, College of Life and Natural Sciences; University of Derby; UK DE22 1GB and Centre for Glaciology, Department of Geography and Earth Sciences; Aberystwyth University; SY 23 3DA |
| File | File Access Level Restricted |
| File | File Access Level Restricted |
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Ody, Helen, Bulling, Mark T. and Barnes, Kate M. 2017. Effects of environmental temperature on oviposition behavior in three blow fly species of forensic importance. Forensic Science International. https://doi.org/10.1016/j.forsciint.2017.03.001An Introduction to Molecular Ecology
Rowe, G., Sweet, M. and Trevor Beebee 2017. An Introduction to Molecular Ecology. Oxford University Press.Nocturnal oviposition behavior of forensically important Diptera in Central England
Barnes, Kate M., Grace, Karon A. and Bulling, Mark T. 2015. Nocturnal oviposition behavior of forensically important Diptera in Central England. Journal of Forensic Sciences. https://doi.org/10.1111/1556-4029.12841Microbial effects on the development of forensically important blow fly species
Crooks, Esther R., Bulling, Mark T. and Barnes, Kate M. 2016. Microbial effects on the development of forensically important blow fly species. Forensic Science International. https://doi.org/10.1016/j.forsciint.2016.05.026Symbiotic microbes from marine invertebrates: Driving a new era of natural product drug discovery.
Blockley, Alix, Elliott, D., Roberts, Adam and Sweet, Michael J. 2017. Symbiotic microbes from marine invertebrates: Driving a new era of natural product drug discovery. Diversity. 9 (4), pp. 1-13. https://doi.org/10.3390/d9040049Designer reefs and coral probiotics; great concepts but are they good practice?
Sweet, M., Ramsey, A. and Bulling, M. 2017. Designer reefs and coral probiotics; great concepts but are they good practice? Biodiversity. https://doi.org/10.1080/14888386.2017.1307786Inducing broadcast coral spawning ex situ: Closed system mesocosm design and husbandry protocol.
Craggs, Jamie, Guest, James R., Davis, Michelle, Simmons, Jeremy, Dashti, Ehsan and Sweet, Michael J. 2017. Inducing broadcast coral spawning ex situ: Closed system mesocosm design and husbandry protocol. Ecology and Evolution. https://doi.org/10.1002/ece3.3538Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera
Sweet, Michael J., Brown, Barbara E., Dunne, Richard P., Singleton, Ian and Bulling, Mark T. 2017. Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera. Coral Reefs. https://doi.org/10.1007/s00338-017-1572-yThe “resort effect”: Can tourist islands act as refuges for coral reef species?
Charlotte Moritz, Frédéric Ducarme, Sweet, M., Michael D. Fox, Brian Zgliczynski, Nizam Ibrahim, Ahmed Basheer, Kathryn A. Furby, Zachary R. Caldwell, Chiara Pisapia, Gabriel Grimsditch and Ameer Abdulla 2017. The “resort effect”: Can tourist islands act as refuges for coral reef species? Diversity and Distributions. https://doi.org/10.1111/ddi.12627On the importance of the microbiome and pathobiome in coral health and disease
Sweet, M. and Bulling, M. 2017. On the importance of the microbiome and pathobiome in coral health and disease. Frontiers in Marine Sciences. https://doi.org/10.3389/fmars.2017.00009'Yellow Syndrome' in scleractinian corals throughout Bintain District, Kepulauan Riau Province, Indonesia
Johan, O., Budianto, O. and Sweet, M. 2017. 'Yellow Syndrome' in scleractinian corals throughout Bintain District, Kepulauan Riau Province, Indonesia. Indonesia Aquaculture Journal. 12 (1), pp. 37-42. https://doi.org/10.15578/iaj.12.1.2017.37-42Variation in size frequency distribution of coral populations under different fishing pressures in two contrasting locations in the Indian Ocean.
Grimsditch, Gabriel, Pisapia, Chiara, Huck, M., Karisa, Juliet, Obura, David and Sweet, M. 2017. Variation in size frequency distribution of coral populations under different fishing pressures in two contrasting locations in the Indian Ocean. Marine Environmental Research. https://doi.org/10.1016/j.marenvres.2017.09.017Juvenile “black teatfish” in Maldives
Sweet, M., Ducarme, F. and Conand, C. 2016. Juvenile “black teatfish” in Maldives. SPC Beche-de-mer Information Bulletin #36. pp. 1-2.Coral responses to anthropogenic stress in the twenty-first century: an ecophysiological perspective
Sweet, M. and Brown B.E. 2016. Coral responses to anthropogenic stress in the twenty-first century: an ecophysiological perspective. in: Oceanography and Marine Biology CRC Press. pp. 271 - 314Is Acropora palmata recovering? A case study in Los Roques National Park, Venezula
Aldo Croquer, Francoise Cavada-Blanco, Ainhoa L Zubillaga, Esteban A Agudo-Adriani and Sweet, M. 2016. Is Acropora palmata recovering? A case study in Los Roques National Park, Venezula. PeerJ. (eCollection 2016). https://doi.org/10.7717/peerj.1539Baseline reef health surveys at Bangka Island (North Sulawesi, Indonesia) reveal new threats
Massimo Ponti, Francesca Fratangeli, Nicolò Dondi, Marco Segre Reinach, Clara Serra and Sweet, M. 2016. Baseline reef health surveys at Bangka Island (North Sulawesi, Indonesia) reveal new threats. PeerJ. https://doi.org/10.7717/peerj.2614The role of viruses in coral health and disease
Sweet, M. and John Bythell 2016. The role of viruses in coral health and disease. Journal of Invertebrate Biology. https://doi.org/10.1016/j.jip.2016.12.005Molecular changes in skin pigmented lesions of the coral trout Plectropomus leopardus
Adélaïde Lerebours, Emma C Chapman, Sweet, M., Jeanette M Rotchell and Michelle R Heupel 2016. Molecular changes in skin pigmented lesions of the coral trout Plectropomus leopardus. Marine Environmental Research. https://doi.org/10.1016/j.marenvres.2016.07.009Influence of Resource Availability on the Foraging Strategies of the Triangle Butterflyfish Chaetodon triangulum in the Maldives
Sweet, M. 2016. Influence of Resource Availability on the Foraging Strategies of the Triangle Butterflyfish Chaetodon triangulum in the Maldives. PLos ONE. https://doi.org/10.1371/journal.pone.0151923New disease outbreak affects two dominant sea urchin species associated with Australian temperate reefs
Sweet, M. and Bulling, M. 2016. New disease outbreak affects two dominant sea urchin species associated with Australian temperate reefs. Marine Ecological Progress Series. https://doi.org/10.3354/meps11750A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs
Martin Stelfox, Jillian Hudgins and Sweet, M. 2016. A review of ghost gear entanglement amongst marine mammals, reptiles and elasmobranchs. Marine Pollution Bulletin. https://doi.org/10.1016/j.marpolbul.2016.06.034Is Acropora Palmata recovering? A case study in Los Roques National Park, Venezuela
Croquer, Aldo, Cavada-Blanco, Francoise, Zubillaga, Ainhoa L., Agudo-Adriani, Esteban A. and Sweet, Michael J. 2016. Is Acropora Palmata recovering? A case study in Los Roques National Park, Venezuela. PeerJ. https://doi.org/10.7717/peerj.1539Coral responses to anthropogenic stress in the 21st Century – An ecophysiological perspective.
Sweet, Michael J. and Brown, Barbara E. 2016. Coral responses to anthropogenic stress in the 21st Century – An ecophysiological perspective. in: Taylor & Francis.Prevalence and Incidence of Black Band Disease of Scleractinian Corals in the Kepulauan Seribu Region of Indonesia
Johan, Ofri, Zamany, Neviaty P., Smith, David and Sweet, M. 2016. Prevalence and Incidence of Black Band Disease of Scleractinian Corals in the Kepulauan Seribu Region of Indonesia. Diversity. https://doi.org/10.3390/d8020011Microbial communities associated with healthy and white syndrome-affected Echinopora lamellose in aquaria and experimental treatment with the antibiotic ampicillin
Smith, D., Leary, P., Craggs, J., Bythell, J. and Sweet, M. 2015. Microbial communities associated with healthy and white syndrome-affected Echinopora lamellose in aquaria and experimental treatment with the antibiotic ampicillin. PLos ONE. 10 (3), pp. 1-17. https://doi.org/10.1371/journal.pone.0121780Identification of a bacterial pathogen associated with Porites white patch syndrome in the Western Indian Ocean
Mathieu G Séré, Pablo Tortosa, Pascale Chabanet, Jean-Pascal Quod, Sweet, M. and Michael H Schleyer 2015. Identification of a bacterial pathogen associated with Porites white patch syndrome in the Western Indian Ocean. Molecular Ecology. https://doi.org/10.1111/mec.13326Ciliate communities consistently associated with coral diseases
Sweet, Michael J. and Séré, Mathieu G. 2015. Ciliate communities consistently associated with coral diseases. Journal of Sea Research. https://doi.org/10.1016/j.seares.2015.06.008Fostering effective international collaboration for marine science in small island states
Hind, Edward J., Alexander, Steven M., Green, Stephanie J., Kritzer, Jacob P., Sweet, M., Johnson, Ayana Elizabeth, Amargós, Fabian P., Smith, Nicola S. and Angelie M. 2015. Fostering effective international collaboration for marine science in small island states. Frontiers in Marine Science. https://doi.org/10.3389/fmars.2015.00086Geographically conserved rates of background mortality among common reef-building corals in Lhaviyani Atoll, Maldives versus northern Great Barrier Reef, Australia
Sweet, M. 2015. Geographically conserved rates of background mortality among common reef-building corals in Lhaviyani Atoll, Maldives versus northern Great Barrier Reef, Australia. Marine Biology. 162 (8). https://doi.org/10.1007/s00227-015-2694-9Diseases in marine invertebrates associated with mariculture and commercial fisheries
Sweet, M. and Kelly S Bateman 2015. Diseases in marine invertebrates associated with mariculture and commercial fisheries. Journal of Sea Research. https://doi.org/10.1016/j.seares.2015.06.016Age-Related Shifts in Bacterial Diversity in a Reef Coral
Alex D Williams, Barbara E Brown, Lalita Putchim and Sweet, M. 2015. Age-Related Shifts in Bacterial Diversity in a Reef Coral. PLos ONE. 10 (2). https://doi.org/10.1371/journal.pone.0144902A novel sponge disease caused by a consortium of micro-organisms
Sweet, M. 2015. A novel sponge disease caused by a consortium of micro-organisms. Coral Reefs. https://doi.org/10.1007/s00338-015-1284-0Baseline coral disease surveys within three marine parks in Sabah, Borneo
Jennifer Miller, Sweet, M., Elizabeth Wood and John Bythell 2015. Baseline coral disease surveys within three marine parks in Sabah, Borneo. PeerJ. https://doi.org/10.7717/peerj.1391White Syndrome in Acropora muricata: Non-specific bacterial infection and ciliate histophagy
Sweet, M. and Bythell, J. 2015. White Syndrome in Acropora muricata: Non-specific bacterial infection and ciliate histophagy. Molecular Ecology. 24, p. 1150–1159. https://doi.org/10.1111/mec.13097The distribution and abundance of black band disease and white syndrome in Kepulauan Seribu, Indonesia
Johan, Ofri, Bengen, Dietriech Geoffrey, Zamani, Neviaty Putri, Suharsono and Sweet, M. 2015. The distribution and abundance of black band disease and white syndrome in Kepulauan Seribu, Indonesia. Journal of Biosciences. https://doi.org/10.1016/j.hjb.2015.09.001Soil contamination with silver nanoparticles reduces Bishop pine growth and ectomycorrhizal diversity on pine roots
Sweet, M. and I Singleton 2015. Soil contamination with silver nanoparticles reduces Bishop pine growth and ectomycorrhizal diversity on pine roots. Journal of Nanoparticle Research. https://doi.org/10.1007/s11051-015-3246-4A novel investigation of a blister-like syndrome in aquarium Echinopora lamellosa
David Smith, Peter Leary, Mark Bendall, Edmund Flach, Rachel Jones and Sweet, M. 2014. A novel investigation of a blister-like syndrome in aquarium Echinopora lamellosa. PLos ONE. https://doi.org/10.1371/journal.pone.0097018Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis
Sweet, M., A Croquer and J C Bythell 2014. Experimental antibiotic treatment identifies potential pathogens of white band disease in the endangered Caribbean coral Acropora cervicornis. Proc Roy Soc. https://doi.org/10.1098/rspb.2014.0094Decadal environmental ‘memory’ in a reef coral?
Brown B.E., Dunne R.P., Edwards A.J., Sweet, M. and Phongsuwan N. 2014. Decadal environmental ‘memory’ in a reef coral? Marine Biology. https://doi.org/10.1007/s00227-014-2596-2Coral diseases in aquaria and in nature
Sweet, Michael J., Jones, Rachel and Bythell, John C. 2013. Coral diseases in aquaria and in nature. https://doi.org/10.1017/S0025315411001688Development of bacterial biofilms on artificial corals in comparison to surface-associated microbes of hard corals
Sweet, Michael J., Croquer, Aldo, Bythell, John C. and Lopez-Garcia, Purification 2013. Development of bacterial biofilms on artificial corals in comparison to surface-associated microbes of hard corals. https://doi.org/10.1371/journal.pone.0021195Characterisation of the bacterial and fungal communities associated with different lesion sizes of Dark Spot Syndrome occurring in the Coral Stephanocoenia intersepta
Sweet, Michael J., Burn, Deborah, Croquer, Aldo, Leary, Peter and Bereswill, Stefan 2013. Characterisation of the bacterial and fungal communities associated with different lesion sizes of Dark Spot Syndrome occurring in the Coral Stephanocoenia intersepta. https://doi.org/10.1371/journal.pone.0062580Evidence of melanoma in wild marine fish populations
Sweet, Michael J., Kirkham, Nigel, Bendall, Mark, Currey, Leanne, Bythell, John C., Heupel, Michelle and Vartanian, Jean-Pierre 2013. Evidence of melanoma in wild marine fish populations. https://doi.org/10.1371/journal.pone.0041989Metal-based nanoparticles; size, function and areas for advancement
Sweet, Michael J. 2013. Metal-based nanoparticles; size, function and areas for advancement. in:Using model systems to address the biodiversity-ecosystem functioning process
Bulling, Mark T., White, Piran C. L., Raffaelli, D. and Pierce, Graham J. 2013. Using model systems to address the biodiversity-ecosystem functioning process.How biodiversity affects ecosystem processes: implications for ecological revolutions and benthic ecosystem function
Solan, Martin, Batty, P., Bulling, Mark T. and Godbold, J. A. 2013. How biodiversity affects ecosystem processes: implications for ecological revolutions and benthic ecosystem function. Aquatic Biology. https://doi.org/10.3354/ab00058Global patterns of bioturbation intensity and mixed depth of marine soft sediments
Teal, L. R., Bulling, Mark T., Parker, E. R. and Solan, Martin 2013. Global patterns of bioturbation intensity and mixed depth of marine soft sediments. Aquatic Biology. https://doi.org/10.3354/ab00052Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity
Langenheder, Silke, Bulling, Mark T., Solan, Martin, Prosser, James I. and Bell, Thomas 2013. Bacterial biodiversity-ecosystem functioning relations are modified by environmental complexity. PLos ONE. https://doi.org/10.1371/journal.pone.0010834Impact of biodiversity-climate futures on primary production and metabolism in a model benthic estuarine system
Hicks, Natalie, Bulling, Mark T., Solan, Martin, Raffaelli, D., White, Piran C. L. and Paterson, David M. 2013. Impact of biodiversity-climate futures on primary production and metabolism in a model benthic estuarine system. BMC Ecology. https://doi.org/10.1186/1472-6785-11-7Role of functionally dominant species in varying environmental regimes: evidence for the performance-enhancing effect of biodiversity
Langenheder, Silke, Bulling, Mark T., Prosser, James I. and Solan, Martin 2013. Role of functionally dominant species in varying environmental regimes: evidence for the performance-enhancing effect of biodiversity. BMC Ecology. https://doi.org/10.1186/1472-6785-12-14Funding begets biodiversity
Ahrends, Antje, Burgess, Neil D., Gereau, Roy E., Marchant, Rob, Bulling, Mark T., Lovett, Jon C., Platts, Philip J., Kindemba, Victoria Wilkins, Owen, Nisha, Fanning, Eibleis and Rahbek, Carsten 2013. Funding begets biodiversity. Diversity and Distributions. https://doi.org/10.1111/j.1472-4642.2010.00737.xConservation and the botanist effect
Ahrends, Antje, Rahbek, Carsten, Bulling, Mark T., Burgess, Neil D., Platts, Philip J., Lovett, Jon C., Kindemba, Victoria Wilkins, Owen, Nisha, Sallu, Albert Ntemi and Marshall, Andrew R. 2013. Conservation and the botanist effect. Biological Conservation. https://doi.org/10.1016/j.biocon.2010.08.008Habitat structure mediates biodiversity effects on ecosystem properties
Godbold, J. A., Bulling, Mark T. and Solan, Martin 2013. Habitat structure mediates biodiversity effects on ecosystem properties. Proceedings of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rspb.2010.2414Permeability of intertidal sandflats: impact of temporal variability on sediment metabolism
Zetzche, E., Bulling, Mark T. and Witte, U. 2013. Permeability of intertidal sandflats: impact of temporal variability on sediment metabolism.Modelling the impact of vaccination on tuberculosis in badgers.
Hardstaff, Joanne L., Bulling, Mark T., Marion, Glenn, Hutchings, Michael R. and White, Piran C. L. 2013. Modelling the impact of vaccination on tuberculosis in badgers. Epidemiology and infection. https://doi.org/10.1017/S0950268813000642Indirect effects of non-lethal predation on bivalve activity and sediment reworking
Maire, O., Merchant, J. N., Bulling, Mark T., Teal, L. R., Grémare, A., Duchêne, J. C. and Solan, Martin 2013. Indirect effects of non-lethal predation on bivalve activity and sediment reworking. Journal of Experimental Marine Biology and Ecology. https://doi.org/10.1016/j.jembe.2010.08.004Predictable waves of sequential forest degradation and biodiversity loss spreading from an African city
Ahrends, Antje, Burgess, Neil D., Milledge, Simon A. H., Bulling, Mark T., Fisher, Brendan, Smart, James C. R., Clarke, G. P., Mhoro, Boniface E. and Lewis, Simon L. 2013. Predictable waves of sequential forest degradation and biodiversity loss spreading from an African city. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.0914471107Geographical variation in the response to nitrogen deposition in Arabidopsis lyrata petraea.
Vergeer, Philippine, van den Berg, Leon L. J., Bulling, Mark T., Ashmore, Mike R. and Kunin, William E. 2008. Geographical variation in the response to nitrogen deposition in Arabidopsis lyrata petraea. The new phytologist. https://doi.org/10.1111/j.1469-8137.2008.02445.xMarine biodiversity-ecosystem functions under uncertain environmental futures
Bulling, Mark T., Hicks, Natalie, Murray, L., Paterson, David M., Raffaelli, D., White, Piran C. L. and Solan, Martin 2013. Marine biodiversity-ecosystem functions under uncertain environmental futures. Philosophical Transactions of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rstb.2010.0022Species effects on ecosystem processes are modified by faunal responses to habitat composition.
Bulling, Mark T., Solan, Martin, Dyson, Kirstie E., Hernandez-Milian, Gema, Luque, Patricia, Pierce, Graham J., Raffaelli, D., Paterson, David M. and White, Piran C. L. 2008. Species effects on ecosystem processes are modified by faunal responses to habitat composition. Oecologia. https://doi.org/10.1007/s00442-008-1160-5Influence of macrofaunal assemblages and environmental heterogeneity on microphytobenthic production in experimental systems
Dyson, Kirstie E., Bulling, Mark T., Solan, Martin, Hernandez-Milian, Gema, Raffaelli, D., White, Piran C. L. and Paterson, David M. 2013. Influence of macrofaunal assemblages and environmental heterogeneity on microphytobenthic production in experimental systems. Proceedings of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rspb.2007.0922Quantifying individual feeding variability: implications for mollusc feeding experiments
Hanley, M. E., Bulling, Mark T. and Fenner, M. 2013. Quantifying individual feeding variability: implications for mollusc feeding experiments.