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Vertical Structure of Heterotrophic Bacterioplankton Communities in the Western Pacific Ocean

Eleanor S. Austria1,2,3,4*, Chun-Wei Chang2,3,4, Ku-Wai Wang2, Joan S. Awingan1, Kuo-Yuan Li2, and Fuh-Kwo Shiah2

1Biology Department, Adamson University, 900 San Marcelino St., Ermita, Manila, Philippines
2Research Center for Environmental Changes, Academia Sinica, Taipei, Taiwan
3Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan
4National Central University, Zhongli, Taiwan

*Corresponding author: This email address is being protected from spambots. You need JavaScript enabled to view it.

 


ABSTRACT

The abundance and composition of summer heterotrophic bacterioplankton communities at the Western Pacific Ocean (WPO) were determined using catalyzed-reporter deposition-fluorescence in situ hybridization (CARD-FISH) technique. Several oligonucleotide probes specific to the Domain Bacteria (EUB338), Phylum Proteobacteria (α-, β-, and γ-Proteobacteria and SAR 11); Actinobacteria (HGC); and Cytophaga-Flavobacter-Bacteroides (CFB) were used to identify and quantify the common bacterial phyla relative to total microbial abundance using  4’ 6-diamidino-2-phenylindole (DAPI) over a depth profile – from 10 to 4000 m. The profiles of microbial and bacterial abundance, temperature, and oxygen all decreased with depth, in contrast to the profiles of the inorganic compounds.  Around 30–59% of the DAPI-positive cells took up the EUB338 probe, suggesting that bacteria are numerically significant components of the microbial biomass in the WPO. Phylum Proteobacteria was the predominant group in the whole water column, with classes α-and γ-Proteobacteria and SAR 11 numerically dominating at specific depths. Statistical analyses showed an association between the bacterial groups – α-Proteobacteria and CFB – and the environmental parameters – temperature and chlorophyll-a concentration – at the depth of 100 m, suggesting the role of organic matter and temperature in structuring the bacterial community in this oceanic regime. This study provided a preview on the abundance and controls of specific groups of heterotrophic bacteria in the WPO, warranting a more detailed and comprehensive investigation of the community structure at clade or genus level.

 

INTRODUCTION

Heterotrophic bacterioplankton, herein referred to as bacteria, are microscopic organisms that play major roles in the biogeochemical cycling of nutrients in aquatic systems. They are responsible for the mineralization of organic compounds, processing more than 50% of the phytoplankton-produced organic matter in the water column (Biddanda 1988). In addition, they convert these non-living organic compounds into biomass that then enters the food chain. This central role in carbon cycling is emphasized in the microbial loop, a concept that links the bacterial conversion of dissolved organic compounds (DOC) into biomass for the higher trophic levels (Jiao & Zheng 2011). . . . . read more

 

REFERENCES

ALM EW, OERTHER DB, LARSEN N., STAHL DA, RASKIN L. 1996. The oligonucleotide probe database. Appl Environ Microbiol 62: 3557–59.
AUSTRIA E, LAI CC, KO CY, LEE KY, KUO H Y. CHEN TY, TAI JH, SHIAH FK. 2018. Growth-controlling mechanisms on heterotrophic bacteria in the South China Sea shelf: Summer and winter patterns. Terrestrial Atmospheric and Oceanic Sciences 29: 1–13.
BECKER J, BERUBE P, FOLLETT C, WATERBURY J, CHISHOLM S, DELONG E, REPETA D. 2014. Closely related phytoplankton species produce similar suites of dissolved organic matter. Frontiers in Microbiology 5.
BIDDANDA B. 1988. Microbial aggregation and degradation of phytoplankton-derived detritus in seawater. II. Microbial metabolism. . Mar Ecol Prog 42: 89–95.
BOUVIER T, DEL GIORGIO PA. 2003. Factors influencing the detection of bacterial cells using fluorescence in situ hybridization (FISH): A quantitative review of published reports. Fems Microbiology Ecology 44: 3–15.
CARINI P, VAN MOOY BA, THRASH JC, WHITE A, ZHAO Y, CAMPBELL EO, FREDRICKS HF, GIOVANNONI SJ. 2015. SAR11 lipid renovation in response to phosphate starvation. Proc Natl Acad Sci USA 112: 7767–72.
CASEY JR, FALKOWSKI PG, KARL DM. 2015. Substrate selection for heterotrophic bacterial growth in the sea. Marine Chemistry 177: 349–356.
DAIMS H, LÜCKER S, WAGNER MS. 2006. Daime, a novel image analysis program for microbial ecology and biofilm research. Environ Microbiol 8: 200–213.
DE CORTE D, SINTES E, YOKOKAWA T, LEKUNBERRI I, HERNDL GJ. 2016. Large-scale distribution of microbial and viral populations in the South Atlantic Ocean. Environmental Microbiology Reports 8: 305–315.
DELMONT TO, QUINCE C, SHAIBER A, ESEN ÖC, LEE STM, RAPPÉ MS, MCLELLAN SL, LÜCKER S, EREN AM. 2018. Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes. Nature Microbiology 3: 804–813.
DENNIS PG, SEYMOUR J, KUMBUN K, TYSON GW. 2013. Diverse populations of lake water bacteria exhibit chemotaxis towards inorganic nutrients. The ISME Journal 7: 1661–64.
EILERS H, PERNTHALER J, GLÖCKNER FO, AMANN R. 2000. Culturability and In Situ Abundance of Pelagic Bacteria from the North Sea. Applied and Environmental Microbiology 66: 3044–51.
FREITAS S, HATOSY S, FUHRMAN JA, HUSE SM, WELCH DB, SOGIN ML, MARTINY AC. 2012. Global distribution and diversity of marine Verrucomicrobia. ISME J 6: 1499–1505.
GILBERT JA, STEELE JA, CAPORASO J, STEINBRU È, REEDER J, TEMPERTON B. 2012. Defining seasonal marine microbial community dynamics. ISME J 6: 298–308.
GIOVANNONI SJ. 2017. SAR11 Bacteria: The Most Abundant Plankton in the Oceans. Annual Review of Marine Science 9: 231–255.
HATOSY SM, MARTINY JB, SACHDEVA R, STEELE J, FUHRMAN JA, MARTINY A C. 2013. Beta diversity of marine bacteria depends on temporal scale. Ecology 94: 1898–1904.
HERLEMANN DPR, LABRENZ M, JUERGENS K, BERTILSSON S, WANIEK JJ, ANDERSSON AF. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. Isme Journal 5: 1571–79.
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. Applied and Environmental Microbiology 71: 2303–09.
HOIKKALA L, TAMMERT H, LIGNELL R, ERONEN-RASIMUS E, SPILLING K, KISAND V. 2016. Autochthonous Dissolved Organic Matter Drives Bacterial Community Composition during a Bloom of Filamentous Cyanobacteria. Frontiers in Marine Science 3.
JIAO NZ, ZHENG Q. 2011. The Microbial Carbon Pump: from Genes to Ecosystems. Applied and Environmental Microbiology 77: 7439–44.
KARNER MB, DELONG EF, KARL DM. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507.
KIRCHMAN DL 2002. The ecology of Cytophaga–Flavobacteria in aquatic environments. Fems Microbiology Ecology 39: 91–100.
LANGENHEDER S, JURGENS K. 2001. Regulation of bacterial biomass and community structure by metazoan and protozoan predation. Limnology and Oceanography 46: 121–134.
LANGENHEDER S, LINDSTROM ES, TRANVIK LJ. 2006. Structure and function of bacterial communities emerging from different sources under identical conditions. Applied and Environmental Microbiology 72: 212–220.
LEE C, WAKEHAM S, ARNOSTI C. 2004. Particulate organic matter in the sea: The composition conundrum. Ambio 33: 565–575.
LOGUE JB, STEDMON CA, KELLERMAN AM, NIELSEN NJ, ANDERSSON AF, LAUDON H, LINDSTROM ES, KRITZBERG ES. 2016. Experimental insights into the importance of aquatic bacterial community composition to the degradation of dissolved organic matter. ISME Journal 10: 533–545.
LONGNECKER K, LOMAS MW, VAN MOOY BA. 2010. Abundance and diversity of heterotrophic bacterial cells assimilating phosphate in the subtropical North Atlantic Ocean. Environ Microbiol 12: 2773–82.
MANTI AP, BOI P, SEMPRUCCI F, CATAUDELLA R, PAPA S. 2012. Picoplankton Community Composition by CARD-FISH and Flow Cytometric Techniques: A Preliminary Study in Central Adriatic Sea Water. International Journal of Oceanography 2012.
MIZUNO CM, RODRIGUEZ-VALERA F, GHAI R. 2015. Genomes of Planktonic  Acidimicrobiales: Widening Horizons for Marine Actinobacteria by Metagenomics. mBio 6.
PARSONS T, MAITA Y, LALLI C. 1984. A Manual of Chemical & Biological Methods for Seawater Analysis. Pergamon Press.
PERNTHALER A, PERNTHALER J. 2007. Fluorescence in Situ Hybridization for the Identification of Environmental Microbes. In: Hilario E, Mackay J eds. Protocols for Nucleic Acid Analysis by Nonradioactive Probes. Totowa, NJ (US): Humana Press. p. 153–164.
PIZZETTI I, FUCHS BM, GERDTS G, WICHELS A, WILTSHIRE KH, AMANN R. 2011. Temporal Variability of Coastal Planctomycetes Clades at Kabeltonne Station, North Sea. Applied and Environmental Microbiology 77: 5009–17.
SALAZAR G, SUNAGAWA S. 2017. Marine microbial diversity. Current Biology 27: R489–R494.
SEO J-H, KANG I, YANG S-J, CHO J-C. 2017. Characterization of spatial distribution of the bacterial community in the South Sea of Korea. PLoS ONE 12: e0174159.
SHIAH FK, WU TH, LI KY, KAO SJ, TSENG YF, CHUNG JL, JAN S. 2006. Thermal effects on heterotrophic processes in a coastal ecosystem adjacent to a nuclear power plant. Marine Ecology Progress Series 309: 55–65.
SPERLING M, PIONTEK J, ENGEL A, WILTSHIRE KH, NIGGEMANN J, GERDTS G, WICHELS A. 2017. Combined Carbohydrates Support Rich Communities of Particle-Associated Marine Bacterioplankton. Frontiers in Microbiology 8.
WARD AC, BORA N. 2006. Diversity and biogeography of marine Actinobacteria. Current Opinion in Microbiology 9: 279–286.
WEBSTER NS, TAYLOR MW, BEHNAM F, LÜCKER S, RATTEI T, WHALAN S, HORN M, WAGNER M. 2010. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environmental Microbiology 12: 2070–82.
WILLIAMS TJ, WILKINS D, LONG E, EVANS F, DEMAERE MZ, RAFTERY MJ, CAVICCHIOLI R. 2013. The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ Microbiol 15: 1302–17.