Abstract
In the present study, we used catalyzed reporter deposition-fluorescence in situ hybridization to quantify the abundance of five bacterial (Alphaproteobacteria, SAR11, Gammaproteobacteria, SAR86, and Bacteroidetes) and two archaeal (Crenarchaeota and Euryarchaeota) phylotypes in the epipelagic layer (0–200 m) of the Central South Pacific Ocean along 170°W from 0° to 40°S. We found that the distribution patterns of these phylotypes differed from each other. All phylotypes except Gammaproteobacteria were particularly abundant at the surface water of the equatorial region, whereas Gammaproteobacteria was relatively abundant in the area from the southern part of the South Pacific Ocean. SAR11, affiliated with Alphaproteobacteria was the dominant phylotype at all depths, throughout the study area. The abundance of SAR11 significantly increased with chlorophyll a concentration, suggesting that phytoplankton could affect their distribution pattern. There was a positive correlation between Bacteroidetes abundance and water temperature, suggesting that the temperature gradient could be a critical factor determining their distribution in the South Pacific Ocean. Crenarchaeota and Euryarchaeota were more abundant at the equatorial region than in other study areas. Euryarchaeota abundance significantly decreased with depth, and increased with chlorophyll a concentration. This suggests that there was ecological interaction between Euryarchaeota and phytoplankton in the equatorial surface. Our data indicate that distinct hydrographic properties such as seawater temperature, salinity, and the concentrations of chlorophyll a and nutrients can principally control the basin-scale distribution of different prokaryotic phylotypes in the epipelagic layer of the Central South Pacific Ocean.
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References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19(6):716–723
Amann R, Fuchs BM (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat Rev Microbiol 6(5):339–348
Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56(6):1919–1925
Bauer M, Kube M, Teeling H, Richter M, Lombardot T, Allers E, Würdemann CA, Quast C, Kuhl H, Knaust F, Woebken D, Bischof K, Mussmann M, Choudhuri JV, Meyer F, Reinhardt R, Amann RI, Glöckner FO (2006) Whole genome analysis of the marine Bacteroidetes ‘Gramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ Microbiol 8(12):2201–2213
Beman JM, Popp BN, Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2(4):429–441
Campbell BJ, Waidner LA, Cottrell MT, Kirchman DL (2008) Abundant proteorhodopsin genes in the North Atlantic Ocean. Environ Microbiol 10(1):99–109
Cho JC, Giovannoni SJ (2004) Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 70(1):432–440
Cho JC, Stapels MD, Morris RM, Vergin KL, Schwalbach MS, Givan SA, Barofsky DF, Giovannoni SJ (2007) Polyphyletic photosynthetic reaction centre genes in oligotrophic marine Gammaproteobacteria. Environ Microbiol 9(6):1456–1463
del Giorgio PA, Gasol JM (2008) Physiological structure and single-cell activity in marine Bacterioplankton. In: Kirchman DL (ed) Microbial ecology of the oceans, 2nd edn. Wiley, Hoboken, pp 243–298
Díez-Vives C, Gasol JM, Acinas SG (2014) Spatial and temporal variability among marine Bacteroidetes populations in the NW Mediterranean Sea. Syst Appl Microbiol 37(1):68–78
Dupont CL, Rusch DB, Yooseph S, Lombardo MJ, Richter RA, Valas R, Novotny M, Yee-Greenbaum J, Selengut JD, Haft DH, Halpern AL, Lasken RS, Nealson K, Friedman R, Venter JC (2012) Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J 6(6):1186–1199
Eiler A, Hayakawa DH, Church MJ, Karl DM, Rappé MS (2009) Dynamics of the SAR11 bacterioplankton lineage in relation to environmental conditions in the oligotrophic North Pacific subtropical gyre. Environ Microbiol 11(9):2291–2300
Eilers H, Pernthaler J, Glöckner FO, Amann R (2000) Culturability and In situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66(7):3044–3051
Fazi S, Amalfitano S, Piccini C, Zoppini A, Puddu A, Pernthaler J (2008) Colonization of overlaying water by bacteria from dry river sediments. Environ Microbiol 10(10):2760–2772
Fernández-Gómez B, Richter M, Schüler M, Pinhassi J, Acinas SG, González JM, Pedrós-Alió C (2013) Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7(5):1026–1037
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102(41):14683–14688
Galand PE, Lovejoy C, Pouliot J, Vincent WF (2008) Heterogeneous archaeal communities in the particle-rich environment of an arctic shelf ecosystem. J Mar Syst 74(3):774–782
Galand PE, Gutiérrez-Provecho C, Massana R, Gasol JM, Casamayor EO (2010) Inter-annual recurrence of archaeal assemblages in the coastal NW Mediterranean Sea (Blanes Bay Microbial Observatory). Limnol Oceanogr 55(5):2117–2125
Godfrey JS, Cresswell GR, Golding TJ, Pearce AF, Boyd R (1980) The separation of the East Australian current. J Phys Oceanogr 10:430–440
Gómez-Consarnau L, González JM, Coll-Lladó M, Gourdon P, Pascher T, Neutze R, Pedrós-Alió C, Pinhassi J (2007) Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445(7124):210–213
Gómez-Pereira PR, Fuchs BM, Alonso C, Oliver MJ, van Beusekom JE, Amann R (2010) Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J 4(4):472–487
González JM, Fernández-Gómez B, Fernàndez-Guerra A, Gómez-Consarnau L, Sánchez O, Coll-Lladó M, del Campo J, Escudero L, Rodríguez-Martínez R, Alonso-Sáez L, Latasa M, Paulsen I, Nedashkovskaya O, Lekunberri I, Pinhassi J, Pedrós-Alió C (2008) Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proc Natl Acad Sci USA 105(25):8724–8729
González JM, Pinhassi J, Fernández-Gómez B, Coll-Lladó M, González-Velázquez M, Puigbò P, Jaenicke S, Gómez-Consarnau L, Fernàndez-Guerra A, Goesmann A, Pedrós-Alió C (2011) Genomics of the proteorhodopsin-containing marine flavobacterium Dokdonia sp. strain MED134. Appl Environ Microbiol 77(24):8676–8686
Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7(6):860–873
Hama T, Miyazaki T, Ogawa Y, Iwakuma T, Takahashi M, Otsuki A, Ichimura S (1983) Measurement of photosynthetic production of a marine phytoplankton population using a stable 13C isotope. Mar Biol 73(1):31–36
Hasumi T, Nagata T (2014) Modeling the global cycle of marine dissolved organic matter and its influence on marine productivity. Ecol Model 288(24):9–24
Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C, Pernthaler A, Pernthaler J (2005) Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71(5):2303–2309
Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H, Welsh R, Ye W, González JM, Mace K, Joye SB, Kiene RP, Whitman WB, Moran MA (2006) Bacterial taxa that limit sulfur flux from the ocean. Science 314(5799):649–652
Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335(6068):587–590
Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409(6819):507–510
Kirchman DL, Elifantz H, Dittel AI, Malmstrom RR, Cottrell MT (2007) Standing stocks and activity of Archaea and Bacteria in the Western Arctic Ocean. Limnol Oceanogr 52(2):495–507
Könneke M, Bernhard AE, José R, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437(7058):543–546
Lefort T, Gasol JM (2013) Global-scale distributions of marine surface bacterioplankton groups along gradients of salinity, temperature, and chlorophyll: a meta-analysis of fluorescence in situ hybridization studies. Aquat Microb Ecol 70:111–130
Longhurst AR (2010) Ecological geography of the sea, 2nd edn. Academic, New York
Malmstrom RR, Straza TRA, Cottrell MT, Kirchman DL (2007) Diversity, abundance, and biomass production of bacterial groups in the Western Arctic Ocean. Aquat Microb Ecol 47:45–55
Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15(4):593–600
Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment. Microbiology 142(5):1097–1106
Mary I, Cummings D, Biegala I, Burkill P, Archer S, Zubkov M (2006) Seasonal dynamics of bacterioplankton community structure at a coastal station in the Western English Channel. Aquat Microb Ecol 42:119–126
Massana R, Murray AE, Preston CM, DeLong EF (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63(1):50–56
Moore JK, Doney SC, Glover DM, Fung IY (2001) Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Res Part 2 Top Stud Oceanogr 49(2002):463–507
Morris RM, Vergin KL, Cho J-C, Rappé MS, Carlson CA, Giovannoni SJ (2005) Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time-series Study site. Limnol Oceanogr 50(5):1687–1696
Morris RM, Frazar CD, Carlson CA (2012) Basin-scale patterns in the abundance of SAR11 subclades, marine Actinobacteria (OM1), members of the Roseobacter clade and OCS116 in the South Atlantic. Environ Microbiol 14(5):1133–1144
Neef A (1997) Anwendung der in situ-Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen. Dissertation, Technische Universität München
Nelson CE, Carlson CA (2012) Tracking differential incorporation of dissolved organic carbon types among diverse lineages of Sargasso Sea bacterioplankton. Environ Microbiol 14(6):1500–1516
Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, Howard EC, King E, Oakley CA, Reisch CR, Rinta-Kanto JM, Sharma S, Sun S, Varaljay V, Vila-Costa M, Westrich JR, Moran MA (2010) Genome characteristics of a generalist marine bacterial lineage. ISME J 4(6):784–798
Ogawa H, Fukuda R, Koike I (1999) Vertical distributions of dissolved organic carbon and nitrogen in the Southern Ocean—a new high temperature combustion method and a comparison with photo-oxidation. Deep Sea Res Part 1 Oceanogr Res Pap 46(10):1809–1826
Oh H-M, Kwon KK, Kang I, Kang SG, Lee JH, Kim SJ, Cho JC (2010) Complete genome sequence of “Candidatus Puniceispirillum marinum” IMCC1322, a representative of the SAR116 clade in the Alphaproteobacteria. J Bacteriol 192(12):3240–3241
Oke PR, Middleton JH (2000) Nutrient enrichment off Port Stephens: the role of the East Australian Current. Cont Shelf Res 21(2001):587–606
Orsi WD, Smith JM, Wilcox HM, Swalwell JE, Carini P, Worden AZ, Santoro AE (2015) Ecophysiology of uncultivated marine euryarchaea is linked to particulate organic matter. ISME J 9(8):1747–1763
Pernthaler A, Preston CM, Pernthaler J, DeLong EF, Amann R (2002) Comparison of fluorescently labeled oligonucleotide and polynucleotide probes for the detection of pelagic marine Bacteria and Archaea. Appl Environ Microbiol 68(2):661–667
Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrasé C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70(11):6753–6766
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rappé MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418(6898):630–633
Riemann L, Steward GF, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66(2):578–587
Schattenhofer M, Fuchs BM, Amann R, Zubkov MV, Tarran GA, Pernthaler J (2009) Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environ Microbiol 11(8):2078–2093
Shiozaki T, Furuya K, Kodama T, Takeda S (2009) Contribution of N2 fixation to new production in the western North Pacific Ocean along 155°E. Mar Ecol Prog Ser 377:19–32
Spring S, Riedel T (2013) Mixotrophic growth of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria is carbon-starvation independent and correlates with the type of carbon source and oxygen availability. BMC Microbiol 13(1):117
Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N,N-dimethylformamide. J Oceanogr 46(4):190–194
Tada Y, Taniguchi A, Nagao I, Miki T, Uematsu M, Tsuda A, Hamasaki K (2011) Differing growth responses of major phylogenetic groups of marine bacteria to natural phytoplankton blooms in the western North Pacific Ocean. Appl Environ Microbiol 77(12):4055–4065
Tada Y, Taniguchi A, Sato-Takabe Y, Hamasaki K (2012) Growth and succession patterns of major phylogenetic groups of marine bacteria during a mesocosm diatom bloom. J Oceanogr 68:509–519
Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glöckner FO, Schweder T, Amann R (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336(6081):608–611
Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ (2004) Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and archaea in the deep ocean. Appl Environ Microbiol 70(7):4411–4414
Teira E, Lebaron P, Van Aken H, Herndl GJ (2006a) Distribution and activity of Bacteria and Archaea in the deep water masses of the North Atlantic. Limnol Oceanogr 51:2131–2144
Teira E, Van Aken H, Veth C, Herndl GJ (2006b) Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnol Oceanogr 51:60–69
Tilburg CE, Hurlburt HE, O’Brien JJ, Shriver JF (2001) The dynamics of the East Australian current system: the Tasman front, the East Auckland current, and the East Cape current. J Phys Oceanogr 31:2917–2943
Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA, Giovannoni SJ (2009) Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3(10):1148–1163
Varela MM, Van Aken HM, Sintes E, Herndl GJ (2008) Latitudinal trends of Crenarchaeota and Bacteria in the meso-and bathypelagic water masses of the Eastern North Atlantic. Environ Microbiol 10(1):110–124
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSG, Chan PP, Gollabgir A, Hemp J, Hügler M, Karr EA, Könneke M, Shin M, Lawton TJ, Lowe T, Martens-Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine Crenarchaea. Proc Natl Acad Sci USA 107(19):8818–8823
Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14(2):136–143
Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39(8):1985–1992
West NJ, Obernosterer I, Zemb O, Lebaron P (2008) Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environ Microbiol 10(3):738–756
Wietz M, Gram L, Jørgensen B, Schramm A (2010) Latitudinal patterns in the abundance of major marine bacterioplankton groups. Aquat Microb Ecol 61:179–189
Yan S, Fuchs BM, Lenk S, Harder J, Wulf J, Jiao NZ, Amann R (2009) Biogeography and phylogeny of the NOR5/OM60 clade of Gammaproteobacteria. Syst Appl Microbiol 32(2):124–139
Yokokawa T, Yang Y, Motegi C, Nagata T (2013) Large-scale geographical variation in prokaryotic abundance and production in meso-and bathypelagic zones of the Central Pacific and Southern Ocean. Limnol Oceanogr 58(1):61–73
Yoshizawa S, Kawanabe A, Ito H, Kandori H, Kogure K (2012) Diversity and functional analysis of proteorhodopsin in marine Flavobacteria. Environ Microbiol 14(5):1240–1248
Acknowledgments
We thank the captain and crew of the R/V Hakuho-maru for their support towards collecting samples for this study during cruise KH-13-7. This study was financially supported by Research Fellowships for Young Scientists (No. 13J04633 and No. 26740001) to Y. T. and Grants-in-Aid (No. 24121004) to K. S. from the Japan Society for the Promotion of Science.
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Tada, Y., Shiozaki, T., Ogawa, H. et al. Basin-scale distribution of prokaryotic phylotypes in the epipelagic layer of the Central South Pacific Ocean during austral summer. J Oceanogr 73, 145–158 (2017). https://doi.org/10.1007/s10872-016-0391-z
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DOI: https://doi.org/10.1007/s10872-016-0391-z