Abstract
Antarctic macroalgae are important primary producers and habitat-forming species that play fundamental roles in Antarctic coastal habitats and sustain important communities of benthic organisms, including a not well-known microbiota. Anthropogenic pressures, e.g., increasing ocean temperatures and extreme events, have threatened the ecological integrity of several seaweed species and also can modify the range shifts (e.g., introduction of Durvillaea antarctica in King George Island), cause local extinctions, and alter the structure of these associations in their natural habitats. However, understanding and prediction of the responses of seaweeds to changing environment and rapid anthropogenic-driven change cannot be done without considering the associated microbiome. These complex microbial communities are intricately involved in the host health, defense, growth, and development of seaweeds, thus with far-reaching implications for the ecology of the whole coastal ecosystem. For most Antarctic seaweeds, the microbiome comprises a stable core as well as microbes whose presence depends on local conditions and transient microbial associates that are responsive to biotic and abiotic processes across spatial and temporal scales. In this chapter, we will explore the ecological and genetic diversity of microbiomes in Antarctic seaweeds and their functional connections.
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Almeida A, Mitchell AL, Tarkowska A, Finn RD (2018) Benchmarking taxonomic assignments based on 16S rRNA gene profiling of the microbiota from commonly sampled environments. Gigascience 7:1–10
Alvarado P, Huang Y, Wang J, Garrido I, Leiva S (2018) Phylogeny and bioactivity of epiphytic gram-positive bacteria isolated from three co-occurring Antarctic macroalgae. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 111:1543–1555
Arnaud-Haond S, Aires T, Candeias R, Teixeira S, Duarte C, Valero M, Serrão E (2017) Entangled fates of holobiont genomes during invasion: nested bacterial and host diversities in Caulerpa taxifolia. Mol Ecol 26:2379–2391
Brodie J, Williamson C, Barker GL, Walker RH, Briscoe A, Yallop M (2016) Characterising the microbiome of Corallina officinalis, a dominant calcified intertidal red alga. FEMS Microbiol Ecol 92:1–12
Bukin YS, Galachyants YP, Morozov IV, Bukin SV, Zakharenko AS, Zemskaya TI (2019) The effect of 16s rRNA region choice on bacterial community metabarcoding results. Sci Data 6:1–14
Burke C, Steinberg P, Rusch DB, Kjelleberg S, Thomas T (2011a) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci U S A 108:14288–14293
Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg (2011b) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600
Busetti A, Maggs CA, Gilmore BF (2017) Marine macroalgae and their associated microbiomes as a source of antimicrobial chemical diversity. Eur J Phycol 52:452–465
Campbell AH, Marzinelli EM, Gelber J, Steinberg PD (2015) Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed. Front Microbiol 6:1–10
Castro-Sowinski S (ed) (2019) The ecological role of micro-organisms in the Antarctic environment. Springer Polar Sciences, Springer, Cham
Chua CY, Yong ST, González MA, Lavin P, Cheah YK, Tan GYA, Wong CMVL (2018) Analysis of bacterial communities of King George and Deception Islands, Antarctica using high-throughput sequencing. Curr Sci 115:1701–1705
Clark MS, Clarke A, Cockell CS, Convey P, Detrich HW, Fraser KPP, Johnston IA, Methe BA et al (2004) Antarctic genomics. Comp Funct Genomics 16:230–238
Clayton MN (1994) Evolution of the Antarctic marine benthic algal flora. J Phycol 30:897–904
De Maayer P, Anderson D, Cary C, Cowan DA (2014) Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep 15:508–517
Dieser M, Greenwood M, Foreman CM (2010) Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arct Antarct Alp Res 42:396–405
Dittami SM, Duboscq-Bidot L, Perennou M, Gobet A, Corre E, Boyen C, Tonon T (2016) Host-microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures. ISME J 10:51–63
Egan S, Gardiner M (2016) Microbial dysbiosis: rethinking disease in marine ecosystems. Front Microbiol 7:1–8
Egan S, James S, Holmström C, Kjelleberg S (2001) Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicata. FEMS Microbiol Ecol 35:67–73
Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol Rev 37:462–476
Egan S, Kumar V, Nappi J, Gardiner M (2017) Microbial diversity and symbiotic interactions with macroalgae. In: Grube M, Seckbach J, Muggia L (eds) Algal and cyanobacteria symbioses. World Scientific Publishing Europe Ltd, London/Singapore, pp 493–546
Flocco C, Cormack W, Smalla K (2019) Antarctic soil microbial communities in a changing environment: their contributions to the sustainability of Antarctic ecosystems and the bioremediation of anthropogenic pollution. In: Castro-Sowinski S (ed) The ecological role of micro-organisms in the Antarctic environment. Springer Polar Sciences, Springer, Cham, pp 133–161
Friedrich MW (2012) Bacterial communities on macroalgae. In: Wiencke C, Bischof K (eds) Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 189–201
Fuks G, Elgart M, Amir A, Zeisel A, Turnbaugh PJ, Soen Y, Shental N (2018) Combining 16S rRNA gene variable regions enables high-resolution microbial community profiling. Microbiome 6:1–13
Furbino LE, Godinho VM, Santiago IF, Pellizari FM, Alves TMA, Zani CL, Junior PAS et al (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microb Ecol 67:775–787
Furbino LE, Pellizzari FM, Neto PC, Rosa CA, Rosa LH (2017) Isolation of fungi associated with macroalgae from maritime Antarctica and their production of agarolytic and carrageenolytic activities. Polar Biol 41:527–535
Gentile G, Giuliano L, D’Auria G, Smedile F, Azzaro M, De Domenico M, Yakimov MM (2006) Study of bacterial communities in Antarctic coastal waters by a combination of 16S rRNA and 16S rDNA sequencing. Environ Microbiol 8:2150–2161
Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R et al (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308
Giudice A, Azzaro M (2019) Diversity and ecological roles of prokaryotes in the changing Antarctic marine environment. In: Castro-Sowinski (ed) the ecological role of micro-organisms in the Antarctic environment. Springer Polar Sciences, Springer, Cham, pp 109–131
Glaeser J, Klug G (2005) Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology 151:1927–1938
Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya NS, Pupo D, Alves TMA, Junior PAS et al (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451
Gómez I, Wulff A, Roleda MY, Huovinen P, Karsten U, Quartino ML, Dunton K, Wiencke C (2009) Light and temperature demands of marine benthic microalgae and seaweeds in polar regions. Bot Mar 52:593–608
Gómez I, Navarro NP, Huovinen P (2019) Bio-optical and physiological patterns in Antarctic seaweeds: a functional trait based approach to characterize vertical zonation. Prog Oceanogr 174:17–27
Hernandez-Agreda A, Leggat W, Bongaerts P, Ainsworth T (2016) The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. MBio 7:1–10
Hollants J, Leliaert F, De Clerck O, Willems A (2013) What we can learn from sushi: a review on seaweed-bacterial associations. FEMS Microbiol Ecol 83:1–16
Hoyer K, Karsten U, Wiencke C (2002) Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar Biol 141:619–627
Huovinen P, Gómez I (2013) Photosynthetic characteristics and UV stress tolerance of Antarctic seaweeds along the depth gradient. Polar Biol 36:1319–1332
Hurd C, Harrison P, Bischof K, Lobban C (eds) (2014) Seaweed ecology and physiology. Cambridge University Press, Cambridge
Janda JM, Abbott SL (2007) 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 45:2761–2764
Kahilainen A, Puurtinen M, Kotiaho JS (2014) Conservation implications of species-genetic diversity correlations. Glob Ecol Conserv 2:315–323
Karsten U, Wulff A, Roleda MY, Müller R, Steinhoff FS, Fredersdorf J, Wiencke C (2009) Physiological responses of polar benthic algae to ultraviolet radiation. Bot Mar 52:639–654
Klöser H, Quartino ML, Wiencke C (1996). Distribution of macroalgae and macroalgal communities in gradients of physical conditions in Potter Cove, King George Island, Antarctica. Hydrobiologia 333: 1–17
Koskella B, Hall LJ, Metcalf CJE (2017) The microbiome beyond the horizon of ecological and evolutionary theory. Nat Ecol Evol 1:1606–1615
Kumar V, Zozaya-Valdes E, Kjelleberg S, Thomas T, Egan S (2016) Multiple opportunistic pathogens can cause a bleaching disease in the red seaweed Delisea pulchra. Environ Microbiol 18:3962–3975
Lachnit T, Blümel M, Imhoff JF, Wahl M (2009) Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat Biol 5:181–186
Lachnit T, Meske D, Wahl M, Harder T, Schmitz R (2011) Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665
Langille M, Zaneveld J, Caporaso J, McDonald D, Knights D, Reyes J, Clemente J et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814
Leiva S, Alvarado P, Huang Y, Wang J, Garrido I (2015) Diversity of pigmented gram-positive bacteria associated with marine macroalgae from Antarctica. FEMS Microbiol Lett 362:1–6
Lemay MA, Martone PT, Hind KR, Lindstrom SC, Wegener-Parfrey L (2018) Alternate life history phases of a common seaweed have distinct microbial surface communities. Mol Ecol 27:3555–3568
Lo Giudice A, Caruso G, Rizzo C, Papale M, Azzaro M (2019) Bacterial communities versus anthropogenic disturbances in the Antarctic coastal marine environment. Environ Sustain 2:297–310
Loque CP, Medeiros AO, Pellizzari FM, Oliveira EC, Rosa CA, Rosa LH (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648
Martin M, Portetelle D, Michel G, Vandenbol M (2014) Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol 98:2917–2935
Martin M, Barbeyron T, Martin R, Portetelle D, Michel G, Vandenbol M (2015) The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria. Front Microbiol 6:1–14
Marx JC, Collins T, D’Amico S, Feller G, Gerday C (2007) Cold-adapted enzymes from marine Antarctic microorganisms. Mar Biotechnol 9:293–304
Marzinelli E, Campbell A, Zozaya E, Vergés A, Nielsen S, Wernberg T, de Bettignies T et al (2015) Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography. Environ Microbiol 17:4078–4088
Moran M (2015) The global ocean microbiome. Science 80:350, aac84551–aac84556
Moreno-Pino M, De la Iglesia R, Valdivia N, Henríquez-Castilo C, Galán A, Díez B, Trefault N (2016) Variation in coastal Antarctic microbial community composition at sub-mesoscale: spatial distance or environmental filtering? FEMS Microbiol Ecol 92:1–13
Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NPA (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments microbiol. Mol Biol Rev 70:222–252
Morris M, Haggerty J, Papudeshi B, Vega A, Edwards M, Dinsdale E (2016) Nearshore pelagic microbial community abundance affects recruitment success of giant kelp, Macrocystis pyrifera. Front Microbiol 7:1–12
Morrissey KL, Çavas L, Willems A, De Clerck O (2019) Disentangling the influence of environment, host specificity and thallus differentiation on bacterial communities in siphonous green seaweeds. Front Microbiol 10:1–12
Ogaki MB, de Paula MT, Ruas D, Pellizzari FM, García-Laviña CX, Rosa LH (2019) Marine fungi associated with Antarctic macroalgae. In: Castro-Sowinski S (ed) The ecological role of micro-organisms in the Antarctic environment. Springer Polar Sciences, Springer, Cham, pp 239–255
Parrot D, Blümel M, Utermann C, Chianese G, Krause S, Kovalev A, Gorb SN, Tasdemir D (2019) Mapping the surface microbiome and metabolome of brown seaweed Fucus vesiculosus by amplicon sequencing, integrated metabolomics and imaging techniques. Sci Rep 9:1–17
Pellizzari F, Silva MC, Silva EM, Medeiros A, Oliveira MC, Yokoya NS, Pupo D, Rosa LH, Colepicolo P (2017) Diversity and spatial distribution of seaweeds in the South Shetland Islands, Antarctica: an updated database for environmental monitoring under climate change scenarios. Polar Biol 40:1671–1685
Pham VHT, Kim J (2012) Cultivation of unculturable soil bacteria. Trends Biotechnol 30:475–484
Pollock J, Glendinning L, Wisedchanwet T, Watson M (2018) The madness of microbiome: attempting to find consensus. Appl Environ Microbiol 84:1–12
Pootakham W, Mhuantong W, Yoocha T, Putchim L, Sonthirod C, Naktang C, Thongtham N, Tangphatsornruang S (2017) High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci Rep 7:1–14
Rausch P, Hermes B, Doms S, Dagan T, Domin H, Fraune S, Humeida UH, Heinsen F, Jahn M, Jaspers C et al (2019) Comparative analysis of amplicon and metagenomic sequencing methods reveals key features in the evolution of animal metaorganisms. Microbiome 7:1–19
Rogers AD (2007) Evolution and biodiversity of Antarctic organisms: a molecular perspective. Philos Trans R Soc B Biol Sci 362:2191–2214
Roth-Schulze AJ, Zozaya-Valdés E, Steinberg PD, Thomas T (2016) Partitioning of functional and taxonomic diversity in surface-associated microbial communities. Environ Microbiol 18:4391–4402
Rout ME (2014) The plant microbiome. In: Paterson AH (ed) Genomes of herbaceous land plants. Advances in Botanical Research. Elsevier Ltd., London, pp 279–309
Saha M, Wiese J, Weinberger F, Wahl M (2016) Rapid adaptation to controlling new microbial epibionts in the invaded range promotes invasiveness of an exotic seaweed. J Ecol 104:969–978
Sambo F, Finotello F, Lavezzo E, Baruzzo G, Masi G, Peta E, Falda M, Toppo S, Barzon L, Di Camillo B (2018) Optimizing PCR primers targeting the bacterial 16S ribosomal RNA gene. BMC Bioinformatics 19:1–10
Serebryakova A, Aires T, Viard F, Serrão EA, Engelen AH (2018) Summer shifts of bacterial communities associated with the invasive brown seaweed Sargassum muticum are location and tissue dependent. PLoS One 13:1–18
Shade A (2016) Diversity is the question, not the answer. ISME J 4:e2287v1
Singh R, Reddy C (2016) Unraveling the functions of the macroalgal microbiome. Front Microbiol 6:1–8
Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160
Tujula NA, Crocetti GR, Burke C, Thomas T, Holmström C, Kjelleberg S (2010) Variability and abundance of the epiphytic bacterial community associated with a green marine ulvacean alga. ISME J 4:301–311
Valdivia N, Díaz MJ, Holtheuer J, Garrido I, Huovinen P, Gómez I (2014) Up, down, and all around: scale-dependent spatial variation in rocky-shore communities of Fildes Peninsula, King George Island, Antarctica. PLoS One 9:1–12
Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206
Wichard T (2015) Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci 6:1–19
Wiencke C, Clayton MN, Gómez I, Iken K, Lüder UH, Amsler CD, Karsten U, Hanelt D, Bischof K, Dunton K (2007) Life strategy, ecophysiology and ecology of seaweeds in polar waters. Rev Environ Sci Biotechnol 6:95–126
Wilkins D, Yau S, Williams TJ, Allen MA, Brown MV, Demaere MZ, Lauro FM, Cavicchioli R (2013) Key microbial drivers in Antarctic aquatic environments. FEMS Microbiol Rev 37:303–335
Acknowledgments
The work outlined in this review was partially supported by the Chilean Antarctic Institute (INACH), the Commonwealth Scientific and Industrial Research Organisation (CSIRO), the University of Hong Kong, and the Institute for Marine and Antarctic Studies (IMAS) from the University of Tasmania. JDGE was supported by the Research Grants Council of Hong Kong via the Early Career Scheme (Project ECS-27124318). MS was funded through the Deutsche Forschungsgemeinschaft (DFG, grant ID: SCHM 3335/1-1).
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Gaitan-Espitia, J.D., Schmid, M. (2020). Diversity and Functioning of Antarctic Seaweed Microbiomes. In: Gómez, I., Huovinen, P. (eds) Antarctic Seaweeds. Springer, Cham. https://doi.org/10.1007/978-3-030-39448-6_14
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