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Shift from Carbon Flow Through the Microbial Loop to the Viral Shunt in Coastal Antarctic Waters During Austral Summer

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Shift from Carbon Flow Through the Microbial Loop to the Viral Shunt in Coastal Antarctic Waters During Austral Summer microorganisms Article Shift from Carbon Flow through the Microbial Loop to the Viral Shunt in Coastal Antarctic Waters during Austral Summer Claire Evans 1,2,*, Joost Brandsma 1,3, Michael P. Meredith 4 , David N. Thomas 5 , Hugh J. Venables 4, David W. Pond 4,6 and Corina P. D. Brussaard 1 1 Royal Netherlands Institute for Sea Research, P.O. Box 59, Den Burg, 1790 AB Texel, The Netherlands; [email protected] (J.B.); [email protected] (C.P.D.B.) 2 Ocean BioGeosciences, National Oceanography Centre, Southampton, European Way, Southampton SO14 3ZH, UK 3 Austere Environments Consortium for Enhanced Sepsis Outcomes, Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD 20814, USA 4 British Antarctic Survey, Natural Environmental Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK; [email protected] (M.P.M.); [email protected] (H.J.V.); [email protected] (D.W.P.) 5 Ecosystems & Environment, Faculty of Biological and Environmental Sciences, University of Helsinki, 00014 Helsinki, Finland; david.thomas@helsinki.fi 6 Faculty of Natural Sciences, University of Stirling, Stirling FK9 4LA, UK * Correspondence: [email protected]; Tel.: +44-(0)2380-596338 Abstract: The relative flow of carbon through the viral shunt and the microbial loop is a pivotal factor controlling the contribution of secondary production to the food web and to rates of nutrient remineralization and respiration. The current study examines the significance of these processes Citation: Evans, C.; Brandsma, J.; in the coastal waters of the Antarctic during the productive austral summer months. Throughout Meredith, M.P.; Thomas, D.N.; the study a general trend towards lower bacterioplankton and heterotrophic nanoflagellate (HNF) Venables, H.J.; Pond, D.W.; Brussaard, C.P.D. Shift from Carbon abundances was observed, whereas virioplankton concentration increased. A corresponding decline Flow through the Microbial Loop to of HNF grazing rates and shift towards viral production, indicative of viral infection, was measured. −1 −1 the Viral Shunt in Coastal Antarctic Carbon flow mediated by HNF grazing decreased by more than half from 5.7 µg C L day on − − Waters during Austral Summer. average in December and January to 2.4 µg C L 1 day 1 in February. Conversely, carbon flow Microorganisms 2021, 9, 460. https:// through the viral shunt increased substantially over the study from on average 0.9 µg C L−1 day−1 doi.org/10.3390/microorganisms in December to 7.6 µg C L−1 day−1 in February. This study shows that functioning of the coastal 9020460 Antarctic microbial community varied considerably over the productive summer months. In early summer, the system favors transfer of matter and energy to higher trophic levels via the microbial Academic Editor: Johannes F. Imhoff loop, however towards the end of summer carbon flow is redirected towards the viral shunt, causing a switch towards more recycling and therefore increased respiration and regeneration. Received: 28 January 2021 Accepted: 18 February 2021 Keywords: prokaryotes; Antarctica; viruses; heterotrophic nanoflagellates; microbial loop; viral Published: 23 February 2021 shunt; carbon; bacteriovory; viral lysis Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction The microbial loop describes the consumption of dissolved organic matter (DOM) by bacteria, which are then grazed by protists providing a route for carbon transfer to higher trophic levels [1,2]. The grazing step is mediated primarily by heterotrophic nanoflagellates Copyright: © 2021 by the authors. (HNFs) which are the key bacteriovores in aquatic environments [3]. The microbial loop Licensee MDPI, Basel, Switzerland. can serve alongside primary production as a carbon source to the food web [4]. Occurring This article is an open access article in parallel is the ‘viral shunt’ whereby microbial hosts are infected and subsequently lysed distributed under the terms and by viruses, which converts their cell biomass to progeny and DOM [5]. In this way carbon conditions of the Creative Commons is directed back into the pool of potential bacterial substrates [6]. Bacterial consumption Attribution (CC BY) license (https:// of the DOM generated by the action of bacteriophages represents a closed trophic loop, creativecommons.org/licenses/by/ whereby matter is recycled at the base of the food chain [7]. 4.0/). Microorganisms 2021, 9, 460. https://doi.org/10.3390/microorganisms9020460 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 460 2 of 13 Microorganisms 2021consumption, 9, 460 of the DOM generated by the action of bacteriophages represents a closed 2 of 12 trophic loop, whereby matter is recycled at the base of the food chain [7]. The amount of carbon from the DOM pool made available to higher trophic levels by The amount of carbon from the DOM pool made available to higher trophic levels the microbial loop will depend principally on the biotic and abiotic factors driving the by the microbial loop will depend principally on the biotic and abiotic factors driving the magnitude of the fluxes of matter assimilated by bacteria in the first instance and bacteria magnitude of the fluxes of matter assimilated by bacteria in the first instance and bacteria consumed by grazers in the second. As bacterial production is controlled primarily by consumed by grazers in the second. As bacterial production is controlled primarily by bottom-up processes (e.g., carbon availability [8]), factors that dictate DOM concentra- bottom-up processes (e.g., carbon availability [8]), factors that dictate DOM concentrations tions such as phytoplankton excretion and cell lysis [9] will have key significance. Bacte- such as phytoplankton excretion and cell lysis [9] will have key significance. Bacterial rial prey availability will in turn influence carbon flow to HNFs, in addition to their spe- prey availability will in turn influence carbon flow to HNFs, in addition to their specific cific grazing rates and levels of HNF standing stock, which are tightly linked to the inten- grazing rates and levels of HNF standing stock, which are tightly linked to the intensity of sity of predation on the HNFs themselves [10]. predation on the HNFs themselves [10]. As with the microbial loop, the net effect of the viral shunt on carbon flow will de- As with the microbial loop, the net effect of the viral shunt on carbon flow will depend pend on a complexon a web complex of factors web ofrelated factors to relatedthe overlying to the overlyingphysiochemical physiochemical conditions conditions [11] [11] and and the ecologythe of ecology viruses, of grazers viruses,, and grazers, their andhosts. their Theoretically, hosts. Theoretically, viral infection viral infectionmay may serve serve to decreaseto decreasecarbon flow carbon to higher flow totrophic higher levels trophic by levelsreducing by reducingbacterial population bacterial population size size through cellthrough lysis. Key cell factors lysis. Keyin the factors net influence in the netof viruses influence on ofcar virusesbon flow on involve carbon flow involve the ecology of theviruses, ecology bacteria of viruses,, and grazers bacteria,—abundance, and grazers—abundance, susceptibility, virus susceptibility, infection virus infection strategy, successionstrategy, rate succession, and grazing rate, feeding and grazing strategies feeding [7,12 strategies–14]. [7,12–14]. As the amount Asof carbon the amount that flows of carbon through that the flows microbial through loop the microbialand the viral loop shunt and theis viral shunt is intimately tied intimatelyto biotic and tied abiotic to biotic conditions and abiotic we thus conditions hypothesize we thus that hypothesize this is likely that to thisbe is likely to be highly variablehighly in regions variable subject in regionsto high subjectseasonal to fluctuations high seasonal such fluctuations as the polar such marine as the polar marine waters. The Antarcticwaters. coastal The Antarctic regions coastalshow pronounced regions show shifts pronounced in the levels shifts of instocks the levels and of stocks and productivity ofproductivity phytoplankton, of phytoplankton,bacterioplankton bacterioplankton,, and virioplankton and [15 virioplankton–18]. However, [15 as– 18]. However, yet no attemptas has yet been no attempt made to has comprehensively been made to comprehensively study the seasonal study dynamics the seasonal of the dynamics of the microbial and viralmicrobial mediation and viral of carbon mediation flow ofin carbonthis environment. flow in this We environment. selected the We surface selected the surface waters of the coastalwaters Western of the coastal Antarctic Western Peninsula Antarctic (WAP) Peninsula as our study (WAP) site as given our study its well site given its well characterized fluctuationscharacterized in environmental fluctuations in and environmental biological conditions. and biological The study conditions. was con- The study was ducted during conductedthe biologically during productive the biologically summer productive months. summer months. 2. Materials and2. Methods Materials and Methods Study site and Studysampling. site The and primary sampling. samplingThe primary site was sampling located in site the was center located of Ry- in the center of ◦ ◦ der Bay (67.570Ryder° S 68.225 Bay° (67.570 W), whichS 68.225 lies atW), the whichnorthern lies end at the of northernMarguerite end Bay of Marguerite on the Bay on the
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