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Discordance Between Resident and Active Bacterioplankton in Free-Living and Particle-Associated Communities in Estuary Ecosystem

  • Microbiology of Aquatic Systems
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Abstract

Bacterioplankton are the major driving force for biogeochemical cycles in estuarine ecosystems, but the communities that mediate these processes are largely unexplored. We sampled in the Pearl River Estuary (PRE) to examine potential differences in the taxonomic composition of resident (DNA-based) and active (RNA-based) bacterioplankton communities in free-living and particle-associated fractions. MiSeq sequencing data showed that the overall bacterial diversity in particle-associated fractions was higher than in free-living communities. Further in-depth analyses of the sequences revealed a positive correlation between resident and active bacterioplankton communities for the particle-associated fraction but not in the free-living fraction. However, a large overlapping of OTUs between free-living and particle-associated communities in PRE suggested that the two fractions may be actively exchanged. We also observed that the positive correlation between resident and active communities is more prominent among the abundant OTUs (relative abundance > 0.2%). Further, the results from the present study indicated that low-abundance bacterioplankton make an important contribution towards the metabolic activity in PRE.

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References

  1. Mao Q, Shi P, Yin K, Gan J, Qi Y (2004) Tides and tidal currents in the Pearl River Estuary. Cont Shelf Res 24:1797–1808. https://doi.org/10.1016/j.csr.2004.06.008

    Article  Google Scholar 

  2. Fontanez KM, Eppley JM, Samo TJ, Karl DM, DeLong EF (2015) Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre. Front Microbiol 6:469. https://doi.org/10.3389/fmicb.2015.00469

    Article  PubMed  PubMed Central  Google Scholar 

  3. Leorri E, Cearreta A, Irabien MJ, Yusta I (2008) Geochemical and microfaunal proxies to assess environmental quality conditions during the recovery process of a heavily polluted estuary: the Bilbao estuary case (N. Spain). Sci Total Environ 396:12–27. https://doi.org/10.1016/j.scitotenv.2008.02.009

    Article  PubMed  CAS  Google Scholar 

  4. Zhang L, Wang L, Yin K, Lü Y, Zhang D, Yang Y, Huang X (2013) Pore water nutrient characteristics and the fluxes across the sediment in the Pearl River estuary and adjacent waters, China. Estuar Coast Shelf Sci 133:182–192. https://doi.org/10.1016/j.ecss.2013.08.028

    Article  CAS  Google Scholar 

  5. Reed HE, Martiny JBH (2012) Microbial composition affects the functioning of estuarine sediments. ISME J 7:868–879. https://doi.org/10.1038/ismej.2012.154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Bernhard AE, Tucker J, Giblin AE, Stahl DA (2007) Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environ. Microbiol. 9:1439–1447. https://doi.org/10.1111/j.1462-2920.2007.01260.x

    Article  PubMed  CAS  Google Scholar 

  7. Hawkins RJ, Purdy KJ (2007) Genotypic distribution of an indigenous model microorganism along an estuarine gradient. FEMS Microbiol. Ecol. 62:187–194. https://doi.org/10.1111/j.1574-6941.2007.00376.x

    Article  PubMed  CAS  Google Scholar 

  8. Garneau MÈ, Vincent WF, Terrado R, Lovejoy C (2009) Importance of particle-associated bacterial heterotrophy in a coastal Arctic ecosystem. J. Mar. Syst. 75:185–197. https://doi.org/10.1016/j.jmarsys.2008.09.002

    Article  Google Scholar 

  9. Eloe EA, Shulse CN, Fadrosh DW, Williamson SJ, Allen EE, Bartlett DH (2011) Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment. Environ. Microbiol. Rep. 3:449–458. https://doi.org/10.1111/j.1758-2229.2010.00223.x

    Article  PubMed  Google Scholar 

  10. Ortega-Retuerta E, Joux F, Jeffrey WH, Ghiglione JF (2013) Spatial variability of particle-attached and free-living bacterial diversity in surface waters from the Mackenzie River to the Beaufort Sea (Canadian Arctic). Biogeosciences 10:2747–2759. https://doi.org/10.5194/bg-10-2747-2013

    Article  Google Scholar 

  11. D'Ambrosio L, Ziervogel K, MacGregor B, Teske A, Arnosti C (2014) Composition and enzymatic function of particle-associated and free-living bacteria: a coastal/offshore comparison. ISME J 8:2167–2179. https://doi.org/10.1038/ismej.2014.67

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Rieck A, Herlemann DPR, Jürgens K, Grossart HP (2015) Particle-associated differ from free-living bacteria in surface waters of the Baltic Sea. Front Microbiol 6:1297. https://doi.org/10.3389/fmicb.2015.01297

    Article  PubMed  PubMed Central  Google Scholar 

  13. Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505. https://doi.org/10.1128/aem.70.3.1494-1505.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Zhang Y, Zhao Z, Dai M, Jiao N, Herndl GJ (2014) Drivers shaping the diversity and biogeography of total and active bacterial communities in the South China Sea. Mol Ecol 23:2260–2274. https://doi.org/10.1111/mec.12739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Cardoso DC, Sandionigi A, Cretoiu MS, Casiraghi M, Stal L, Bolhuis H (2017) Comparison of the active and resident community of a coastal microbial mat. Sci Rep 7:2969. https://doi.org/10.1038/s41598-017-03095-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Gaidos E, Rusch A, Ilardo M (2011) Ribosomal tag pyrosequencing of DNA and RNA from benthic coral reef microbiota: community spatial structure, rare members and nitrogen-cycling guilds. Environ. Microbiol. 13:1138–1152. https://doi.org/10.1111/j.1462-2920.2010.02392.x

    Article  PubMed  Google Scholar 

  17. Campbell BJ, Yu L, Heidelberg JF, Kirchman DL (2011) Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci U S A. 108:12776–12781. https://doi.org/10.1073/pnas.1101405108

    Article  PubMed  PubMed Central  Google Scholar 

  18. Campbell BJ, Kirchman DL (2013) Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J 7:210–220. https://doi.org/10.1038/ismej.2012.93

    Article  PubMed  CAS  Google Scholar 

  19. Yang Y, Chen F, Zhang L, Liu J, Wu S, Kang M (2012) Comprehensive assessment of heavy metal contamination in sediment of the Pearl River Estuary and adjacent shelf. Mar Pollut Bull 64:1947–1955. https://doi.org/10.1016/j.marpolbul.2012.04.024

    Article  PubMed  CAS  Google Scholar 

  20. Dai M, Zhai W, Cai W-J, Callahan J, Huang B, Shang S, Huang T, Li X, Lu Z, Chen W, Chen Z (2008) Effects of an estuarine plume-associated bloom on the carbonate system in the lower reaches of the Pearl River estuary and the coastal zone of the northern South China Sea. Cont Shelf Res 28:1416–1423. https://doi.org/10.1016/j.csr.2007.04.018

    Article  Google Scholar 

  21. Harrison PJ, Yin K, Lee JHW, Gan J, Liu H (2008) Physical–biological coupling in the Pearl River Estuary. Cont Shelf Res 28:1405–1415. https://doi.org/10.1016/j.csr.2007.02.011

    Article  Google Scholar 

  22. Strokal M, Kroeze C, Li L, Luan S, Wang H, Yang S, Zhang Y (2015) Increasing dissolved nitrogen and phosphorus export by the Pearl River (Zhujiang): a modeling approach at the sub-basin scale to assess effective nutrient management. Biogeochemistry 125:221–242. https://doi.org/10.1007/s10533-015-0124-1

    Article  CAS  Google Scholar 

  23. Liu X, Lu X, Chen Y (2011) The effects of temperature and nutrient ratios on Microcystis blooms in Lake Taihu, China: an 11-year investigation. Harmful Algae 10:337–343. https://doi.org/10.1016/j.hal.2010.12.002

    Article  CAS  Google Scholar 

  24. Cao JJ, Lee SC, Ho KF, Zou SC, Fung K, Li Y, Watson JG, Chow JC (2004) Spatial and seasonal variations of atmospheric organic carbon and elemental carbon in Pearl River Delta Region, China. Atmos Environ 38:4447–4456. https://doi.org/10.1016/j.atmosenv.2004.05.016

    Article  CAS  Google Scholar 

  25. Huang S, He S, Xu H, Wu P, Jiang R, Zhu F, Luan T, Ouyang G (2015) Monitoring of persistent organic pollutants in seawater of the Pearl River Estuary with rapid on-site active SPME sampling technique. Environ Pollut 200:149–158. https://doi.org/10.1016/j.envpol.2015.02.016

    Article  PubMed  CAS  Google Scholar 

  26. Cai WJ, Dai M, Wang Y, Zhai W, Huang T, Chen S, Zhang F, Chen Z, Wang Z (2004) The biogeochemistry of inorganic carbon and nutrients in the Pearl River estuary and the adjacent Northern South China Sea. Cont Shelf Res 24:1301–1319. https://doi.org/10.1016/j.csr.2004.04.005

    Article  Google Scholar 

  27. Lu X, Sun S, Zhang YQ, Hollibaugh JT, Mou X (2015) Temporal and vertical distributions of bacterioplankton at the Gray’s Reef National Marine Sanctuary. Appl Environ Microbiol 81:910–917. https://doi.org/10.1128/aem.02802-14

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lebaron P, Servais P, Agogué H, Courties C, Joux F (2001) Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl Environ Microbiol 67:1775–1782. https://doi.org/10.1128/aem.67.4.1775-1782.2001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Kumar PS, Brooker MR, Dowd SE, Camerlengo T (2011) Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS One 6:e20956. https://doi.org/10.1371/journal.pone.0020956

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. https://doi.org/10.1038/ismej.2011.159

    Article  PubMed  CAS  Google Scholar 

  31. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/aem.01541-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141–D145. https://doi.org/10.1093/nar/gkn879

    Article  PubMed  CAS  Google Scholar 

  33. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peňa AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Hulsen T, de Vlieg J, Alkema W (2008) BioVenn—a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:488. https://doi.org/10.1186/1471-2164-9-488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Suzuki S, Kaneko R, Kodama T, Hashihama F, Suwa S, Tanita I, Furuya K, Hamasaki K (2017) Comparison of community structures between particle-associated and free-living prokaryotes in tropical and subtropical Pacific Ocean surface waters. J Oceanogr 73:383–395. https://doi.org/10.1007/s10872-016-0410-0

    Article  CAS  Google Scholar 

  36. Crespo BG, Pommier T, Fernández-Gómez B, Pedrós-Alió C (2013) Taxonomic composition of the particle-attached and free-living bacterial assemblages in the Northwest Mediterranean Sea analyzed by pyrosequencing of the 16S rRNA. Microbiologyopen 2:541–552. https://doi.org/10.1002/mbo3.92

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Simon M, Grossart H-P, Schweitzer B, Ploug H (2002) Microbial ecology of organic aggregates in aquatic ecosystems. Aquat Microb Ecol 28:175–211. https://doi.org/10.3354/ame028175

    Article  Google Scholar 

  38. Garneau MÈ, Vincent WF, Alonso-Sáez L, Gratton Y, Lovejoy C (2006) Prokaryotic community structure and heterotrophic production in a river-influenced coastal arctic ecosystem. Aquat Microb Ecol 42:27–40. https://doi.org/10.3354/ame042027

    Article  Google Scholar 

  39. Fandino LB, Riemann L, Steward GF, Long RA, Azam F (2001) Variations in bacterial community structure during a dinoflagellate bloom analyzed by DGGE and 16S rDNA sequencing. Aquat Microb Ecol 23:119–130. https://doi.org/10.3354/ame023119

    Article  Google Scholar 

  40. Yung CM, Ward CS, Davis KM, Johnson ZI, Hunt DE (2016) Insensitivity of diverse and temporally variable particle-associated microbial communities to bulk seawater environmental parameters. Appl Environ Microbiol 82:3431–3437. https://doi.org/10.1128/aem.00395-16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Hamdan LJ, Jonas RB (2006) Seasonal and interannual dynamics of free-living bacterioplankton and microbially labile organic carbon along the salinity gradient of the Potomac River. Estuar Coast 29:40–53. https://doi.org/10.1007/bf02784697

    Article  CAS  Google Scholar 

  42. Parveen B, Ravet V, Djediat C, Mary I, Quiblier C, Debroas D, Humbert J-F (2013) Bacterial communities associated with Microcystis colonies differ from free-living communities living in the same ecosystem. Environ Microbiol Rep 5:716–724. https://doi.org/10.1111/1758-2229.12071

    Article  PubMed  CAS  Google Scholar 

  43. Zhang BH, Salam N, Cheng J, Li H-Q, Yang J-Y, Zha D-M, Zhang Y-Q, Ai M-J, Hozzein WN, Li W-J (2016) Modestobacter lacusdianchii sp. nov., a phosphate-solubilizing actinobacterium with ability to promote Microcystis growth. PLoS One 11:e0161069. https://doi.org/10.1371/journal.pone.0161069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Nold SC, Zwart G (1998) Patterns and governing forces in aquatic microbial communities. Aquat Ecol 32:17–35. https://doi.org/10.1023/a:1009991918036

    Article  CAS  Google Scholar 

  45. Tamura T (2014) The family Sporichthyaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Actinobacteria. Springer, Berlin, pp 883–888. https://doi.org/10.1007/978-3-642-30138-4_182

    Chapter  Google Scholar 

  46. DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934. https://doi.org/10.4319/lo.1993.38.5.0924

    Article  Google Scholar 

  47. Kirchman DL (2002) The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100. https://doi.org/10.1111/j.1574-6941.2002.tb00910.x

    Article  PubMed  CAS  Google Scholar 

  48. Gomez-Pereira PR, Fuchs BM, Alonso C, Oliver MJ, van Beusekom JEE, Amann R (2010) Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J 4:472–487. https://doi.org/10.1038/ismej.2009.142

    Article  PubMed  CAS  Google Scholar 

  49. Teixeira LM, Merquior VLC (2014) The family Moraxellaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Gammaproteobacteria. Springer, Berlin, pp 443–476. https://doi.org/10.1007/978-3-642-38922-1_245

    Chapter  Google Scholar 

  50. Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T, Žifčáková L, Šnajdr J, Rídl J, Vlček Č, Voříšková J (2011) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6:248–258. https://doi.org/10.1038/ismej.2011.95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (No. 31528001) and Natural Science Foundation of Guangdong Province, China (No. 2016A030312003). W-J Li was also supported by Guangdong Province Higher Vocational Colleges & Schools Pearl River Scholar Funded Scheme (2014).

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  1. Jia-Ling Li and Nimaichand Salam contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou, Guangdong, China

    Jia-Ling Li, Nimaichand Salam, Pan-Deng Wang, Lin-Xing Chen, Jian-Yu Jiao, Xin Li, Wen-Dong Xian, Ming-Xian Han, Bao-Zhu Fang & Wen-Jun Li

  2. Department of Biological Sciences, Kent State University, Kent, OH, USA

    Xiao-Zhen Mou

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Li, JL., Salam, N., Wang, PD. et al. Discordance Between Resident and Active Bacterioplankton in Free-Living and Particle-Associated Communities in Estuary Ecosystem. Microb Ecol 76, 637–647 (2018). https://doi.org/10.1007/s00248-018-1174-4

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