Advertisement

Microbial Ecology

, Volume 76, Issue 3, pp 637–647 | Cite as

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

  • 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
  • Xiao-Zhen MouEmail author
  • Wen-Jun LiEmail author
Microbiology of Aquatic Systems

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.

Keywords

Resident and active community Free-living and particle-associated bacterioplankton Pearl River estuary 

Notes

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).

Supplementary material

248_2018_1174_MOESM1_ESM.docx (333 kb)
ESM 1 (DOCX 332 kb)

References

  1. 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 CrossRefGoogle Scholar
  2. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 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 CrossRefPubMedGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefPubMedGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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 CrossRefPubMedGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 PubMedCrossRefGoogle Scholar
  43. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. 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 PubMedCrossRefGoogle Scholar
  48. 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 CrossRefPubMedGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jia-Ling Li
    • 1
  • Nimaichand Salam
    • 1
  • Pan-Deng Wang
    • 1
  • Lin-Xing Chen
    • 1
  • Jian-Yu Jiao
    • 1
  • Xin Li
    • 1
  • Wen-Dong Xian
    • 1
  • Ming-Xian Han
    • 1
  • Bao-Zhu Fang
    • 1
  • Xiao-Zhen Mou
    • 2
    Email author
  • Wen-Jun Li
    • 1
    Email author
  1. 1.State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life SciencesSun Yat-Sen UniversityGuangzhouChina
  2. 2.Department of Biological SciencesKent State UniversityKentUSA

Personalised recommendations