MICROBIOLOGY OF THE RAPIDLY CHANGING POLAR ENVIRONMENTS EDITED BY : Julie Dinasquet, Eva Ortega-Retuerta, Connie Lovejoy and Ingrid Obernosterer PUBLISHED IN: Frontiers in Marine Science and Frontiers in Microbiology 1 June 2018 | A q u a t i c M i c r o b i o l o g y o f P o l a r E n v i r o n m e n t s F r o n t i e r s i n M a r i n e S c i e n c e Frontiers Copyright Statement © Copyright 2007-2018 Frontiers Media SA. All rights reserved. All content included on this site, such as text, graphics, logos, button icons, images, video/audio clips, downloads, data compilations and software, is the property of or is licensed to Frontiers Media SA (“Frontiers”) or its licensees and/or subcontractors. The copyright in the text of individual articles is the property of their respective authors, subject to a license granted to Frontiers. 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With their unique mix of varied contributions from Original Research to Review Articles, Frontiers Research Topics unify the most influential researchers, the latest key findings and historical advances in a hot research area! Find out more on how to host your own Frontiers Research Topic or contribute to one as an author by contacting the Frontiers Editorial Office: researchtopics@frontiersin.org 2 June 2018 | A q u a t i c M i c r o b i o l o g y o f P o l a r E n v i r o n m e n t s F r o n t i e r s i n M a r i n e S c i e n c e MICROBIOLOGY OF THE RAPIDLY CHANGING POLAR ENVIRONMENTS Marginal ice zone, sea ice and meltwater in the Baffin Bay, Arctic Ocean, June 2016. Image: Julie Dinasquet. Topic Editors: Julie Dinasquet, Scripps Institution of Oceanography, University of California, San Diego, United States Eva Ortega-Retuerta, CNRS, Sorbonne Universities, France Connie Lovejoy, Laval University, Canada Ingrid Obernosterer, CNRS, Sorbonne Universities, France Marine and freshwater polar environments are characterized by intense physical forces and strong seasonal variations. The persistent cold and sometimes inhospitable conditions create unique ecosystems and habitats for microbial life. Polar microbial communities are diverse productive assemblages, which drive biogeochemical cycles and support higher food-webs across the Arctic and over much of the Antarctic. Recent studies on the biogeography of microbial species have revealed phylogenet- ically diverse polar ecotypes, suggesting adaptation to seasonal darkness, sea-ice coverage and high summer irradiance. Because of the diversity of habitats related to atmospheric and oceanic circulation, and the formation and melting of ice, high latitude oceans and lakes are ideal environments to investigate composition and functionality of microbial communities. In addition, polar regions are responding more dramatically to climate change compared to temperate environments and 3 June 2018 | A q u a t i c M i c r o b i o l o g y o f P o l a r E n v i r o n m e n t s F r o n t i e r s i n M a r i n e S c i e n c e there is an urgent need to identify sensitive indicators of ecosystem history, that may be sentinels for change or adaptation. For instance, Antarctic lakes provide useful model systems to study microbial evolution and climate history. Hence, it becomes essential and timely to better understand factors controlling the microbes, and how, in turn, they may affect the functioning of these fragile ecosystems. Polar microbiology is an expanding field of research with exciting possibilities to provide new insights into microbial ecology and evolution. With this Research Topic we seek to bring together polar microbiologists studying different aquatic systems and components of the microbial food web, to stimulate discussion and reflect on these sensitive environments in a changing world perspective. Citation: Dinasquet, J., Ortega-Retuerta, E., Lovejoy, C., Obernosterer, I., eds. (2018). Microbiology of the Rapidly Changing Polar Environments. Lausanne: Frontiers Media. doi: 10.3389/978-2-88945-513-3 4 June 2018 | A q u a t i c M i c r o b i o l o g y o f P o l a r E n v i r o n m e n t s F r o n t i e r s i n M a r i n e S c i e n c e Table of Contents 07 Editorial: Microbiology of the Rapidly Changing Polar Environments Julie Dinasquet, Eva Ortega-Retuerta, Connie Lovejoy and Ingrid Obernosterer CHANGES IN POLAR PHYTOPLANKTON COMMUNITIES DYNAMICS 10 Southern Ocean Phytoplankton in a Changing Climate Stacy L. Deppeler and Andrew T. Davidson 38 Microbial Eukaryotes in an Arctic Under-Ice Spring Bloom North of Svalbard Archana R. Meshram, Anna Vader, Svein Kristiansen and Tove M. Gabrielsen 50 Atlantic Advection Driven Changes in Glacial Meltwater: Effects on Phytoplankton Chlorophyll-a and Taxonomic Composition in Kongsfjorden, Spitsbergen Willem H. van De Poll, Douwe S. Maat, Philipp Fischer, Patrick D. Rozema, Oonagh B. Daly, Sebastiaan Koppelle, Ronald J. W. Visser and Anita G. J. Buma 61 Synechococcus in the Atlantic Gateway to the Arctic Ocean Maria L. Paulsen, Hugo Doré, Laurence Garczarek, Lena Seuthe, Oliver Müller, Ruth-Anne Sandaa, Gunnar Bratbak and Aud Larsen 75 Seasonal and Interannual Changes in Ciliate and Dinoflagellate Species Assemblages in the Arctic Ocean (Amundsen Gulf, Beaufort Sea, Canada) Deo F. L. Onda, Emmanuelle Medrinal, André M. Comeau, Mary Thaler, Marcel Babin and Connie Lovejoy 89 Models of Plankton Community Changes During a Warm Water Anomaly in Arctic Waters Show Altered Trophic Pathways With Minimal Changes in Carbon Export Maria Vernet, Tammi L. Richardson, Katja Metfies, Eva-Maria Nöthig and Ilka Peeken 108 Protist Communities in Moored Long-Term Sediment Traps (Fram Strait, Arctic)–Preservation With Mercury Chloride Allows for PCR-Based Molecular Genetic Analyses Katja Metfies, Eduard Bauerfeind, Christian Wolf, Pim Sprong, Stephan Frickenhaus, Lars Kaleschke, Anja Nicolaus and Eva-Maria Nöthig CHANGES IN POLAR HETEROTROPHIC MICROBIAL COMMUNITIES DYNAMICS 121 A Decadal (2002–2014) Analysis for Dynamics of Heterotrophic Bacteria in an Antarctic Coastal Ecosystem: Variability and Physical and Biogeochemical Forcings Hyewon Kim and Hugh W. Ducklow 139 Seasonal Succession of Free-Living Bacterial Communities in Coastal Waters of the Western Antarctic Peninsula Catherine M. Luria, Linda A. Amaral-Zettler, Hugh W. Ducklow and Jeremy J. Rich 5 June 2018 | A q u a t i c M i c r o b i o l o g y o f P o l a r E n v i r o n m e n t s F r o n t i e r s i n M a r i n e S c i e n c e 152 Changes in Marine Prokaryote Composition With Season and Depth Over an Arctic Polar Year Bryan Wilson, Oliver Müller, Eva-Lena Nordmann, Lena Seuthe, Gunnar Bratbak and Lise Øvreås 169 Unanticipated Geochemical and Microbial Community Structure Under Seasonal Ice Cover in a Dilute, Dimictic Arctic Lake Ursel M. E. Schütte, Sarah B. Cadieux, Chris Hemmerich, Lisa M. Pratt and Jeffrey R. White 184 Microbial Community Structure and Interannual Change in the Last Epishelf Lake Ecosystem in the North Polar Region Mary Thaler, Warwick F. Vincent, Marie Lionard, Andrew K. Hamilton and Connie Lovejoy 199 Changes of the Bacterial Abundance and Communities in Shallow Ice Cores from Dunde and Muztagata Glaciers, Western China Yong Chen, Xiang-Kai Li, Jing Si, Guang-Jian Wu, Li-De Tian and Shu-Rong Xiang 215 Uptake of Leucine, Chitin, and Iron by Prokaryotic Groups During Spring Phytoplankton Blooms Induced by Natural Iron Fertilization off Kerguelen Island (Southern Ocean) Marion Fourquez, Sara Beier, Elanor Jongmans, Robert Hunter and Ingrid Obernosterer 228 Viruses and Protists Induced-Mortality of Prokaryotes Around the Antarctic Peninsula During the Austral Summer Dolors Vaqué, Julia A. Boras, Francesc Torrent-Llagostera, Susana Agustí, Jesús M. Arrieta, Elena Lara, Yaiza M. Castillo, Carlos M. Duarte and Maria M. Sala ARCTIC MICROBIOLOGY 240 Microbial Community Response to Terrestrially Derived Dissolved Organic Matter in the Coastal Arctic Rachel E. Sipler, Colleen T. E. Kellogg, Tara L. Connelly, Quinn N. Roberts, Patricia L. Yager and Deborah A. Bronk 259 Carbon Bioavailability in a High Arctic Fjord Influenced by Glacial Meltwater, NE Greenland Maria L. Paulsen, Sophia E. B. Nielsen, Oliver Müller, Eva F. Møller, Colin A. Stedmon, Thomas Juul-Pedersen, Stiig Markager, Mikael K. Sejr, Antonio Delgado Huertas, Aud Larsen and Mathias Middelboe 278 Upstream Freshwater and Terrestrial Sources are Differentially Reflected in the Bacterial Community Structure Along a Small Arctic River and its Estuary Aviaja L. Hauptmann, Thor N. Markussen, Marek Stibal, Nikoline S. Olsen, Bo Elberling, Jacob Bælum, Thomas Sicheritz-Pontén and Carsten S. Jacobsen 6 June 2018 | A q u a t i c M i c r o b i o l o g y o f P o l a r E n v i r o n m e n t s F r o n t i e r s i n M a r i n e S c i e n c e ANTARCTIC BENTHIC MICROBIOLOGY 294 Biogeochemical and Microbial Variation Across 5500 km of Antarctic Surface Sediment Implicates Organic Matter as a Driver of Benthic Community Structure Deric R. Learman, Michael W. Henson, J. Cameron Thrash, Ben Temperton, Pamela M. Brannock, Scott R. Santos, Andrew R. Mahon and Kenneth M. Halanych 305 High Prevalence of Gammaproteobacteria in the Sediments of Admiralty Bay and North Bransfield Basin, Northwestern Antarctic Peninsula Diego C. Franco, Camila N. Signori, Rubens T. D. Duarte, Cristina R. Nakayama, Lúcia S. Campos and Vivian H. Pellizari EDITORIAL published: 04 May 2018 doi: 10.3389/fmars.2018.00154 Frontiers in Marine Science | www.frontiersin.org May 2018 | Volume 5 | Article 154 Edited by: Jonathan P. Zehr, University of California, Santa Cruz, United States Reviewed by: Patricia Lynn Yager, University of Georgia, United States *Correspondence: Julie Dinasquet jdinasquet@ucsd.edu Specialty section: This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Marine Science Received: 31 December 2017 Accepted: 13 April 2018 Published: 04 May 2018 Citation: Dinasquet J, Ortega-Retuerta E, Lovejoy C and Obernosterer I (2018) Editorial: Microbiology of the Rapidly Changing Polar Environments. Front. Mar. Sci. 5:154. doi: 10.3389/fmars.2018.00154 Editorial: Microbiology of the Rapidly Changing Polar Environments Julie Dinasquet 1,2 *, Eva Ortega-Retuerta 2 , Connie Lovejoy 3 and Ingrid Obernosterer 2 1 Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, United States, 2 Laboratoire d’Océanographie Microbienne, LOMIC, Observatoire Océanologique de Banyuls sur mer, CNRS, Sorbonne Universités, Banyuls sur mer, France, 3 Département de Biologie, Université Laval, Québec, QC, Canada Keywords: Arctic, Antarctica, polar microbiology, aquatic microbiology, climate change Editorial on the Research Topic Microbiology of the Rapidly Changing Polar Environments Polar environments are warming at alarming rates (Tingley and Huybers, 2013; Schmidtko et al., 2014). The rapid warming is a threat to the integrity of these ice-influenced ecosystems, where microbes are the dominant life form (Boetius et al., 2015; Cavicchioli, 2015; Pedros-Alio et al., 2015; Mohit et al., 2017). Polar regions play a crucial role in regulating the climate system, and have acted as an anthropogenic CO 2 sink due to combinations of low temperatures and high gas solubility, high winds, extensive winter sea ice cover, and intense biological productivity (Arrigo et al., 2008; Bates and Mathis, 2009). Despite being geographically distant, the Arctic and the Antarctic aquatic ecosystems have much in common. Both regions are subjected to harsh environmental conditions such as low temperatures and darkness in winter, extreme seasonal shifts in solar radiation, high UV exposure in summer, and seasonal changes in ice cover on both lakes and seas. In spite of this apparent inhospitality, polar aquatic ecosystems host diverse and active microbial communities that drive biogeochemical cycles and support higher trophic levels (Cavicchioli, 2015; Pedros-Alio et al., 2015). Since polar regions are more strongly impacted by global change (Yoshimori et al., 2017) than temperate regions, there is an urgent need to understand how these perturbations will affect microbial functions and major elemental cycles, including carbon. Marine and freshwater high-latitude aquatic environments offer an ideal variety of habitats to investigate changes in the community composition and functionality of aquatic microbes, who may be true sentinels of global change. The microbiology across many habitats in these vulnerable ecosystems are the subject of this special topic in Frontiers in Marine Science and Microbiology (Aquatic Microbiology). The goal of this topic was to bring together contributions that provide a “bi-polar view” of aquatic microbiology. The range of contributions highlights both similar and distinct microbial processes that take place within the two high-latitude extreme environments. This research topic touches upon a wide range of interests to polar microbiologists, and provides a collection of 20 articles, including: a review, in situ observations, experiments, technical notes and modeling studies. While most of the articles focus on the response of bacterial communities to environmental changes, several look into the response of microbial eukaryotes, and others take a more biogeochemical approach that includes examining carbon and nutrient dynamics. Finally, we are proud of the high contribution by women to this research topic (the four scientific editors, 75% of first authors, 47% of all authors, 32% of reviewers), which highlights the important contribution of women to polar science in general and microbial ecology in particular. 7 Dinasquet et al. Aquatic Microbiology of Polar Environments In contrast to lower latitude regions, annual pelagic primary production in polar ecosystems is constrained by relatively short summers. It is during this brief summer period that light conditions are favorable for the phytoplankton growth, but this only can occur if nutrients are available. Recently, earlier spring-retreat of sea ice, along with the decrease in seasonal sea ice cover especially in the Arctic has led to increased light availability, which could increase primary production. However, increased stratification from meltwater may result in decreased nutrient supply to the euphotic zone. Earlier studies suggested that meltwater itself can sometimes increase nutrient supply to the phytoplankton in the Southern Ocean, and that higher winds across the open water in the Arctic could promote fall blooms. Such changes in phytoplankton phenology could have a cascading effect on other biological activities, potentially perturbing the polar carbon cycle. In this special topic, the review by Deppeler and Davidson concluded that long-term changes in Antarctic phytoplankton dynamics will depend on the magnitude and timing of the climate change induced stressors. In the Arctic, Meshram et al. show that under-ice bloom composition is related to both water mass mixing and local processes. Warming also influences melt water inputs and water column stratification, governing bloom intensities and composition, as reported by van De Poll et al. Current and future environmental changes may shift dominant phytoplankton groups toward smaller species (Paulsen et al.; Onda et al.; Vernet et al.). As changes in the relative size of the dominant primary producers appears to favor small mixotrophic species, tools to assess their trophic interactions and carbon fluxes should be developed. The need to establish baselines was raised by Metfies et al. who propose exploiting preserved sediment trap samples using molecular markers to increase the length of records and facilitate comparisons to more recent data. Looking toward future trends, Vernet et al. used a modeling approach to suggest that community changes could be neutral and perhaps may not impact carbon export budgets. In polar aquatic ecosystems, the seasonal dynamics of heterotrophic microbial communities are coupled with phytoplankton blooms that produce pulses of labile organic matter. As part of this research topic, several studies report bacterial responses to seasonal and inter-annual variability. Around the western Antarctic Peninsula, seasonal variation in bacterial activities and communities indicate strong coupling with phytoplankton blooms (Kim and Ducklow; Luria et al.). But bacterial heterotrophic production, key to food web functioning, may be fueled by additional sources of carbon (Kim and Ducklow). In the Arctic Svalbard Archipelago, epipelagic microbial communities are also tightly coupled to phytoplankton blooms while seasonal variations do not appear to affect mesopelagic communities (Wilson et al.). Community changes following seasonal ice cover variability were also observed in epishelf and inland lakes where climate change may have major impacts on biogeochemical cycles (Schütte et al.; Thaler et al.). Similar seasonal responses are also observed in alpine glacier ecosystems (Chen et al.). The studies mentioned above, suggest that polar and cold climate microbial communities should be closely monitored as means to anticipate future effects and potential feedback loops on polar ecosystem functioning. Shifts in heterotrophic microbial communities may also reflect specific community capacities to use seasonal pulses of resources, such as organic carbon and iron, and induce microbial interactions (Fourquez et al.). Vaqué et al. demonstrated that viral infection is more sensitive to climate change and warming compared to grazing, implying that not only variation in community composition and activity, but also bacterial mortality agents will affect the fate of the carbon fluxes through microbial food webs. Whereas, similar responses to seasonal variability are observed between the Arctic and the Antarctic, future changes may amplify differences between these regions. Compared to the Southern Ocean, the Arctic is largely surrounded by land masses and with large river inputs ( ∼ 4,000 km 3 yr − 1 ). These rivers are a source of low-salinity waters, organic matter, and nutrients to the Arctic Ocean and surrounding seas. Moreover, as temperature rises, terrestrial permafrost thaws, which mobilizes ancient carbon that enters the ocean through freshwater discharge. Here, Sipler et al. show that this terrestrial and riverine organic matter is rapidly degraded by bacterial activity even before reaching open waters suggesting a need to revisit the notion that this carbon should be considered as mainly refractory (Kirchman et al., 2009). Nevertheless, phytoplankton derived organic matter remains a major source of carbon fuelling Arctic bacterial production in spring and summer (Paulsen et al.). But as the Arctic warms and freshwater discharge increases, associated pulses of organic matter supplementing bacterial carbon demand (Paulsen et al.; Sipler et al.) may push Arctic microbial communities toward heterotrophy (Paulsen et al.). Increasing riverine input is also associated with changes in bacterial community structure, as specific organisms respond to the terrestrial derived organic matter (Sipler et al.). Hauptmann et al. point out that the transport of freshwater communities into the coastal marine waters could also affect the functioning of the arctic carbon cycle. Compared to the Southern Ocean, the Arctic Ocean is a semi-closed system, with limited exchanges, through inflow and outflow gateways, with neighboring oceans. Of concern is the recent increase in Atlantic inflow into the European Arctic Ocean (Polyakov et al., 2017), which has been attributed to climate change. The northward intrusion of warmer waters may affect the spring bloom dynamics (van De Poll et al.; Vernet et al.) and favor the establishment of organisms previously absent from these waters, such as the cyanobacterium Synechoccocus (Paulsen et al.). Hence, changes in ocean circulation can have major effects on the biology of the pelagic ecosystem. Lastly, polar benthic ecosystems are not likely to be spared from climate changes as seasonal shifts in surface communities are associated with microbial communities in the sediments (Learman et al.; Franco et al.). An increase in phytoplankton biomass and subsequent carbon export could cause microbial communities in polar sediments to switch from predominantly Frontiers in Marine Science | www.frontiersin.org May 2018 | Volume 5 | Article 154 8 Dinasquet et al. Aquatic Microbiology of Polar Environments lithotrophs to organic matter degraders, which will in turn affect benthic elemental cycles (Learman et al.). While Arctic sea ice extent breaks record lows, and Arctic and Antarctic ice shelves collapse, it is urgent to understand how these dramatic changes will impact the microbial ecology and potentially disrupt the capacity for carbon storage in polar regions. Overall, the studies published in this research topic confirm that major changes already occurring in aquatic polar ecosystems will impact microbial communities, and further suggest that some microbes are potential indicators of these changes. Because most of these studies focus on biodiversity, however, it remains a challenge to unravel how these community changes will alter ecosystem function. Some of the present results hint toward major changes in carbon fluxes and trophic interactions, stressing the need for increased spatial and seasonal coverage, including winter sampling of microbial communities, and continued focus on top-down and bottom up controls of microbial processes. Long-term monitoring is needed to facilitate reliable predictions on how polar aquatic systems will interact with climate and better assess the resilience and adaptation of these fragile ecosystems. Moreover, as polar microbial communities are fundamental to carbon cycling, informed modeling approaches that integrate polar microbial complexity are needed to understand the implications of climate change. AUTHOR CONTRIBUTIONS All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. FUNDING This work was supported by the Marie Curie Actions- International Outgoing Fellowship (PIOF-GA-2013-629378) to JD and Intra-European Fellowship (H2020-MSCA-IF-2015- 703991) to EO-R. CL acknowledges support from the Canadian Natural Science and Engineering Council (NSERC) discovery program and the Canada First Research Excellence Fund supporting Sentinel North. ACKNOWLEDGMENTS We would like to thank the editorial staff at Frontiers in marine sciences and in aquatic microbiology for their initial invitation and support throughout. REFERENCES Arrigo, K. R., Van Dijken, G., and Long, M. (2008). 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The role of atmospheric heat transport and regional feedbacks in the Arctic warming at equilibrium. Clim. Dyn. 49:3457. doi: 10.1007/s00382-017-3523-2 Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer PLY declared a past co-authorship with one of the authors, JD, to the handling Editor. Copyright © 2018 Dinasquet, Ortega-Retuerta, Lovejoy and Obernosterer. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Frontiers in Marine Science | www.frontiersin.org May 2018 | Volume 5 | Article 154 9 REVIEW published: 16 February 2017 doi: 10.3389/fmars.2017.00040 Frontiers in Marine Science | www.frontiersin.org February 2017 | Volume 4 | Article 40 Edited by: Julie Dinasquet, University of California, San Diego, USA Reviewed by: Ian Salter, Alfred Wegener Institute for Polar and Marine Research, Germany Bernard Quéguiner, Aix-Marseille University, France *Correspondence: Stacy L. Deppeler stacy.deppeler@utas.edu.au Specialty section: This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Marine Science Received: 30 September 2016 Accepted: 02 February 2017 Published: 16 February 2017 Citation: Deppeler SL and Davidson AT (2017) Southern Ocean Phytoplankton in a Changing Climate. Front. Mar. Sci. 4:40. doi: 10.3389/fmars.2017.00040 Southern Ocean Phytoplankton in a Changing Climate Stacy L. Deppeler 1 * and Andrew T. Davidson 2, 3 1 Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia, 2 Australian Antarctic Division, Department of the Environment and Energy, Kingston, TAS, Australia, 3 Antarctic Climate and Ecosystem Cooperative Research Centre (ACE CRC), University of Tasmania, Hobart, TAS, Australia Phytoplankton are the base of the Antarctic food web, sustain the wealth and diversity of life for which Antarctica is renowned, and play a critical role in biogeochemical cycles that mediate global climate. Over the vast expanse of the Southern Ocean (SO), the climate is variously predicted to experience increased warming, strengthening wind, acidification, shallowing mixed layer depths, increased light (and UV), changes in upwelling and nutrient replenishment, declining sea ice, reduced salinity, and the southward migration of ocean fronts. These changes are expected to alter the structure and function of phytoplankton communities in the SO. The diverse environments contained within the vast expanse of the SO will be impacted differently by climate change; causing the identity and the magnitude of environmental factors driving biotic change to vary within and among bioregions. Predicting the net effect of multiple climate-induced stressors over a range of environments is complex. Yet understanding the response of SO phytoplankton to climate change is vital if we are to predict the future state/s of the ecosystem, estimate the impacts on fisheries and endangered species, and accurately predict the effects of physical and biotic change in the SO on global climate. This review looks at the major environmental factors that define the structure and function of phytoplankton communities in the SO, examines the forecast changes in the SO environment, predicts the likely effect of these changes on phytoplankton, and considers the ramifications for trophodynamics and feedbacks to global climate change. Predictions strongly suggest that all regions of the SO will experience changes in phytoplankton productivity and community composition with climate change. The nature, and even the sign, of these changes varies within and among regions and will depend upon the magnitude and sequence in which these environmental changes are imposed. It is likely that predicted changes to phytoplankton communities will affect SO biogeochemistry, carbon export, and nutrition for higher trophic levels. Keywords: Southern Ocean, phytoplankton, climate change, primary productivity, Antarctica 1. INTRODUCTION Iconic Antarctic wildlife from krill to whales, seals, penguins, and seabirds, ultimately depend on single-celled marine plants (phytoplankton) for their food. More than 500 species of protist have been identified in Antarctic waters, ∼ 350 of which are phytoplankton and ∼ 150 microheterotrophs (Scott and Marchant, 2005, http://taxonomic.aad.gov.au). These organisms coexist with untold numbers of heterotrophic prokaryotes (bacteria and Archaea) and viruses. Together they comprise the microbial food web ( Figure 1 ), through which much of the carbon sequestered by phytoplankton is consumed, respired, and/or remineralized (Azam et al., 1983, 10 Deppeler and Davidson Southern Ocean Phytoplankton in a Changing Climate FIGURE 1 | Schematic showing the connections amongst members of the microbial food web and microbial loop and the processes driving carbon transfer to higher trophic levels and flux to the deep ocean. 1991; Fenchel, 2008; Kirchman, 2008). This food web includes the microbial loop in which dissolved carbon substrates fuel the growth of bacteria and Archaea, which are subsequently consumed by protists, returning carbon to the microbial food web that is otherwise lost to the dissolved pool (Azam et al., 1983). Phytoplankton are the base of the Southern Ocean (SO) food web. In nutrient rich Antarctic coastal waters their blooms can reach concentrations approaching 10 8 cells l − 1 . Chlorophyll a (Chl a ) concentrations as high as 50 μ g l − 1 have been recorded off the West Antarctic Peninsula (WAP), although maximum Chl a concentrations off East Antarctica are usually an order of magnitude less (Nelson et al., 1987; Smith and Gordon, 1997; Wright and van den Enden, 2000; Garibotti et al., 2003; Wright et al., 2010; Goldman et al., 2015). The majority of phytoplankton production in the SO is grazed by microheterotrophs or consumed and remineralized by bacteria (Lochte et al., 1997; Christaki et al., 2014). Production that escapes these fates sinks to depth, often in the form of dead cells, aggregates of biogenic material (marine snow), or fecal pellets, sequestering carbon in the deep ocean. Abbreviations: SO, Southern Ocean; SAZ, sub-Antarctic zone; POOZ, permanently open ocean zone; SSIZ, seasonal sea ice zone; MIZ, marginal ice zone; CZ, Antarctic continental shelf zone; DMSP, dimethylsulfoniopropiothetin; DMS, dimethylsulfide; Chl a , Chlorophyll a ; HNLC, high nutrient, low chlorophyll; UCDW, upper circumpolar deep water; SAM, Southern Annular Mode; WAP, west Antarctic peninsula; ASL, Amundsen Sea Low; ENSO, El Niño-Southern Oscillation; SIE, sea ice extent; CCM, carbon concentrating mechanism; PAR, photosynthetically active radiation; UV, ultraviolet. Some phytoplankton, such as prymnesiophytes and dinoflagellates, also synthesize substantial quantities of dimethylsulfoniopropiothetin (DMSP), which when enzymatically cleaved, forms dimethylsulfide (DMS). Oxidation of DMS in the atmosphere forms sulfate aerosols, which nucleate cloud formation and increase the reflectance of solar radiation (Charlson et al., 1987). The microbial food web plays a vital role in metabolizing these sulfur compounds (Kiene et al., 2000; Simó, 2004). The active involvement of phytoplankton in the sequestration and synthesis of climate-active gases (CO 2 ) and biogenic sulfur compounds (DMSP and DMS), plus the mediation of the fate of these compounds by protozoa and bacteria means that microbes are a crucial determinant of future global climate ( Figure 1 ). The SO plays a substantial role in mediating global climate. The world’s oceans have taken up between 25 and 30% of the anthropogenic CO 2 released to the atmosphere, with ∼ 40% of this uptake occurring in the SO (Raven and Falkowski, 1999; Sabine et al., 2004; Khatiwala et al., 2009; Takahashi et al., 2009; Frölicher et al., 2015). Without this, the atmospheric CO 2 concentration would be ∼ 50% higher than it is today. Drawdown of CO 2 by phytoplankton photosynthesis and vertical transport of this biologically sequestered carbon to the deep ocean (the biological pump) is responsible for around 10% this uptake (Cox et al., 2000; Siegel et al., 2014). Any climate-induced change in the structure or function of phytoplankton communities is likely to alter the efficiency of the biological pump, with feedbacks to the rate of Frontiers in Marine Science | www.frontiersin.org February 2017 | Volume 4 | Article 40 11 Deppeler and Davidson Southern Ocean Phytoplankton in a Changing Climate climate change (Matear and Hirst, 1999; Le Quéré et al., 2007). The SO is a region of seasonal extremes in productivity that reflect the large fluctuations in the SO environment. In summer, the development of large blooms of phytoplankton support a profusion of Antarctic life. Their metabolic activity also affects biogeochemical cycles in the SO, which in turn can influence the global climate. Whilst their effect on global climate is substantial, their microscopic size means they are intimately exposed to changes in their environment and are also likely to be affected by climate change. Already, climate change is causing the southward migration of ocean fronts, increasing sea surface temperatures, and changes in sea ice cover (Constable et al., 2014). Further changes in temperature, salinity, wind strength, mixed layer depth, sea ice thickness, duration and extent, and glacial ice melt are predicted. These changes are likely to affect the composition, abundance, and productivity of phytoplankton in the SO and feed back to threaten the ecosystem services they provide, namely sustaining biodiversity, fueling the food web and fisheries, and mediating global climate (Moline et al., 2004). The SO is a vast and diverse environment, and hence the effect of climate change on the phytoplankton community is likely to be complex. For the purposes of this review we define the SO as waters south of the Sub-Tropical Front, thereby comprising ∼ 20% of the world’s ocean surface area. We subdivide these waters into five regions that group waters according to the environmental drivers of the phytoplankton community in a similar manner as Tréguer and Jacques (1992) and Sullivan et al. (1988), namely the Sub-Antarctic Zone (SAZ), Permanently Open Ocean Zone (POOZ), Seasonal Sea Ice Zone (SSIZ), Marginal Ice Zone (MIZ), and the Antarctic Continental Shelf Zone (CZ) ( Figure 2 ). Differences in environmental factors (physical, chemical, and biological) and processes (e.g., stratification, mixing, grazing) define the composition, abundance, and productivity of the phytoplankton community, both within and between these regions. Climate change is expected to elicit widespread changes in oceanography in each region, such as the displacement of oceanographic fronts (Sokolov and Rintoul, 2009b), as well as different permutations of climate-induced stressors that may interact synergistically or antagonistically, with either beneficial or detrimental effects on the phytoplankton community (Boyd and Brown, 2015; Boyd et al., 2016). Here we identify the factors and processes that critically affect phytoplankton communities in each region of the SO, consider the impacts of climate change on each of these regions, examine the likely effect of these changes on the phytoplankton inhabiting these waters, and predict the possible repercussions for the Antarctic ecosystem. 2. SUB-ANTARCTIC ZONE The Sub-Antarctic Zone (SAZ) comprises more than half the total area of the SO and inco