Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Bacterial composition and spatiotemporal variation in sediments of Jiaozhou Bay, China

Abstract

Purpose

Although coastal marine sediments harbor diverse bacteria with important ecological and environmental functions, a comprehensive view of their community characteristics is still lacking in typical environments along the China coast. We studied the diversity and composition of bacterial community in the sediment of Jiaozhou Bay and characterized their spatiotemporal patterns, aiming to analyze the effects of geographic heterogeneity, seasonal difference, anthropogenic activity, and eutrophication gradient on the bacterial ecology.

Materials and methods

Sixteen full-length bacterial 16S rRNA gene clone libraries were constructed from the sediment bacteria at four stations (A5, B2, D1, and D7) of Jiaozhou Bay over four seasons (February, May, August, and November). The bacterial diversity and community structure variation were analyzed.

Results and discussion

A total of 1088 16S rRNA gene sequences and 746 distinct operational taxonomic units (OTUs) (at 97 % sequence similarity level) were retrieved from the 16 clone libraries. Libraries of each sample revealed a high diversity, and a total of 17 bacterial phyla were identified. Bacteria lineages Proteobacteria (mostly γ-Proteobacteria and δ-Proteobacteria), Actinobacteria, Bacteroidetes, and Planctomycetes, which are commonly found in marine sediments, were the dominant divisions in our samples. Meanwhile, some uncommon phyla, such as Deinococcus-Thermus and Lentisphaerae, were also detected. Distinct spatial patterns and noticeable seasonal variations of bacteria community were observed, indicating that environmental heterogeneity in spatial variation other than in temporal variation may be more important in determining the bacterial communities. Most of the abundant OTUs were related to sequences retrieved from the heavy-metal-polluted environments, indicating that the Jiaozhou Bay might be influenced by pollution.

Conclusions

The bacterial communities in Jiaozhou Bay sediments are highly diverse. The four typical stations that we chose might experience different anthropogenic effects and eutrophication gradients, which shaped their bacterial community composition. The environment of Jiaozhou Bay may be under pressure exerted by multi-dimension anthropogenic activities. This study provided a novel insight into the bacterial community variations in Jiaozhou Bay, enriching knowledge about ecological bioindicators and mechanisms that maintain bacterial diversity and shape bacterial community composition.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Aguiló-Ferretjans MM, Bosch R, Martín-Cardona C, Lalucat J, Nogales B (2008) Phylogenetic analysis of the composition of bacterial communities in human-exploited coastal environments from Mallorca Island (Spain). Syst Appl Microbiol 31(3):231–240

  2. Allen MA, Goh F, Burns BP, Neilan BA (2009) Bacterial, archaeal and eukaryotic diversity of smooth and pustular microbial mat communities in the hypersaline lagoon of Shark Bay. Geobiology 7(1):82–96

  3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

  4. Bai J, Li H, Zhao Y (2009) Bacterial distribution at different stations in the Northern Yellow Sea. Acta Microbiol Sin 3:343–350

  5. Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55(3):541–555

  6. Bertics VJ, Ziebis W (2009) Biodiversity of benthic microbial communities in bioturbated coastal sediments is controlled by geochemical microniches. ISME J 3(11):1269–1285

  7. Bissett A, Bowman J, Burke C (2006) Bacterial diversity in organically-enriched fish farm sediments. FEMS Microbiol Ecol 55(1):48–56

  8. Bolhuis H, Stal LJ (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME J 5(11):1701–1712

  9. Bowman JP, McCuaig RD (2003) Biodiversity, community structural shifts, and biogeography of prokaryotes within antarctic continental shelf sediment. Appl Environ Microbiol 69(5):2463–2483

  10. Dai J, Song J, Li X, Yuan H, Li N, Zheng G (2007) Environmental changes reflected by sedimentary geochemistry in recent hundred years of Jiaozhou Bay, North China. Environ Pollut 145(3):656–667

  11. Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156(4):457–464

  12. Dang H, Li T, Chen M, Huang G (2008a) Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl Environ Microbiol 74:52–60

  13. Dang H, Ren J, Song L, Sun S, An L (2008b) Diverse tetracycline resistant bacteria and resistance genes from coastal waters of Jiaozhou Bay. Microb Ecol 55(2):237–246

  14. Dang H, Ren J, Song L, Sun S, An L (2008c) Dominant chloramphenicol-resistant bacteria and resistance genes in coastal marine waters of Jiaozhou Bay, China. World J Microbiol Biotechnol 24(2):209–217

  15. Dang H, Zhang X, Sun J, Li T, Zhang Z, Yang G (2008d) Diversity and spatial distribution of sediment cammonia-oxidizing crenarchaeota in response to estuarine and environmental gradients in the Changjiang Estuary and East China Sea. Microbiology 154:2084–2095

  16. Dang H, Li J, Chen M, Li T, Zeng Z, Yin X (2009a) Fine-scale vertical distribution of bacteria in the East Pacific deep-sea sediments determined via 16S rRNA gene T-RFLP and clone library analyses. World J Microbiol Biotechnol 25(2):179–188

  17. Dang H, Wang C, Li J, Li T, Tian F, Jin W, Ding Y, Zhang Z (2009b) Diversity and distribution of sediment NirS-encoding bacterial assemblages in response to environmental gradients in the eutrophied Jiaozhou Bay, China. Microb Ecol 58(1):161–169

  18. Dang H, Chen R, Wang L, Guo L, Chen P, Tang Z, Tian F, Li S, Klotz MG (2010a) Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl Environ Microbiol 76(21):7036–7047. doi:10.1128/aem.01264-10

  19. Dang H, Li J, Chen R, Wang L, Guo L, Zhang Z, Klotz MG (2010b) Diversity, abundance, and spatial distribution of sediment ammonia-oxidizing betaproteobacteria in response to environmental gradients and coastal eutrophication in Jiaozhou Bay, China. Appl Environ Microbiol 76(14):4691–4702

  20. Dang H, Chen R, Wang L, Shao S, Dai L, Ye Y, Guo L, Huang G, Klotz MG (2011) Molecular characterization of putative biocorroding microbiota with a novel niche detection of Epsilon- and Zetaproteobacteria in Pacific Ocean coastal seawaters. Environ Microbiol 13:3059–3074

  21. Dang H, Zhou H, Zhang Z, Yu Z, Hua E, Liu X, Jiao N (2013) Molecular detection of Candidatus Scalindua pacifica and environmental responses of sediment anammox bacterial community in the Bohai Sea, China. PLoS ONE 8:e61330

  22. Danovaro R, Pusceddu A (2007) Biodiversity and ecosystem functioning in coastal lagoons: does microbial diversity play any role? Estuar Coast Shelf Sci 75(1–2):4–12

  23. Deng B, Zhang J, Zhang G, Zhou J (2010) Enhanced anthropogenic heavy metal dispersal from tidal disturbance in the Jiaozhou Bay, North China. Environ Monit Assess 161(1–4):349–358

  24. Durbin AM, Teske A (2011) Microbial diversity and stratification of South Pacific abyssal marine sediments. Environ Microbiol 13(12):3219–3234

  25. Eiler A, Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6(12):1228–1243

  26. Feng B-W, Li X-R, Wang J-H, Hu Z-Y, Meng H, Xiang L-Y, Quan Z-X (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiol Ecol 70(2):236–248

  27. Gao X, Chen C-TA (2012) Heavy metal pollution status in surface sediments of the coastal Bohai Bay. Water Res 46(6):1901–1911

  28. Gobet A, Boer SI, Huse SM, van Beusekom JEE, Quince C, Sogin ML, Boetius A, Ramette A (2012) Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J 6(3):542–553

  29. Hamdan LJ, Coffin RB, Sikaroodi M, Greinert J, Treude T, Gillevet PM (2013) Ocean currents shape the microbiome of Arctic marine sediments. ISME J 7(4):685–696

  30. Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43(1):1–11

  31. Hu H-W, Zhang L-M, Dai Y, Di H-J, He J-Z (2013) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments 13(8):1439–1449

  32. Jackson CR, Weeks AQ (2008) Influence of particle size on bacterial community structure in aquatic sediments as revealed by 16S rRNA gene sequence analysis. Appl Environ Microbiol 74(16):5237–5240

  33. Jing R, Hongyue D, Linsheng S, Song S, Liguo A (2006) Bacterial and cyanobacterial diversities determined by T-RFLP analyses in the Jiaozhou Bay. Acta Oceanol Sin 25(4):113–123

  34. Jorgensen SL, Hannisdal B, Lanzén A, Baumberger T, Flesland K, Fonseca R, Øvreås L, Steen IH, Thorseth IH, Pedersen RB, Schleper C (2012) Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic Mid-Ocean Ridge. Proc Natl Acad Sci 109(42):E2846–E2855

  35. Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, Jørgensen BB, Jetten MSM (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci U S A 102(18):6478–6483

  36. Lachmund C, Köcher B, Manz W, Heininger P (2003) Chemical and microbiological in situ characterization of benthic communities in sediments with different contamination levels. J Soils Sediments 3(3):188–196

  37. Li M, Hong Y, Klotz M, Gu J-D (2010) A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl Microbiol Biotechnol 86(2):781–790

  38. Liu Z, Wei H, Liu G, Zhang J (2004) Simulation of water exchange in Jiaozhou Bay by average residence time approach. Estuar Coast Shelf Sci 61(1):25–35

  39. Liu SM, Zhang J, Chen HT, Zhang GS (2005) Factors influencing nutrient dynamics in the eutrophic Jiaozhou Bay, North China. Prog Oceanogr 66(1):66–85

  40. Liu X, Xiao T, Luan Q, Zhang W, Wang M, Yue H (2011) Bacterial diversity, composition and temporal-spatial variation in the sediment of Jiaozhou Bay, China. Chin J Oceanol Limnol 29(3):576–590

  41. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci 104(27):11436–11440

  42. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73(5):1576–1585

  43. Maidak BL, Cole JR, Lilburn TG, Parker CT Jr, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (ribosomal database project). Nucleic Acids Res 29(1):173–174

  44. Martiny JBH, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial β-diversity depend on spatial scale. Proc Natl Acad Sci 108(19):7850–7854

  45. Michaud L, Di Cello F, Brilli M, Fani R, Lo Giudice A, Bruni V (2004) Biodiversity of cultivable psychrotrophic marine bacteria isolated from Terra Nova Bay (Ross Sea, Antarctica). FEMS Microbiol Lett 230(1):63–71

  46. Ravenschlag K, Sahm K, Knoblauch C, Jørgensen BB, Amann R (2000) Community structure, cellular rRNA content, and activity of sulfate-reducing bacteria in marine arctic sediments. Appl Environ Microbiol 66(8):3592–3602

  47. Ren J, Dang H, Song L, Sun S, An L (2006) Bacterial and cyanobacterial diversities determined by T-RFLP analyses in the Jiaozhou Bay. Acta Oceanologica Sinica 25(4):113–123

  48. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71(3):1501–1506

  49. Shi J, Li G, Wang P (2011) Anthropogenic influences on the tidal prism and water exchanges in Jiaozhou Bay, Qingdao, China. J Coast Res 27(1):57–72

  50. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci 103(32):12115–12120

  51. Sun MY, Dafforn KA, Brown MV, Johnston EL (2012) Bacterial communities are sensitive indicators of contaminant stress. Mar Pollut Bull 64(5):1029–1038

  52. Tang X, Gao G, Qin B, Zhu L, Chao J, Wang J, Yang G (2009) Characterization of bacterial communities associated with organic aggregates in a large, shallow, eutrophic freshwater lake (Lake Taihu, China). Microb Ecol 58(2):307–322

  53. ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide : software for canonical community ordination (version 4.5). Biometris, Wageningen

  54. Vallaeys T, Topp E, Muyzer G, Macheret V, Laguerre G, Rigaud A, Soulas G (1997) Evaluation of denaturing gradient gel electrophoresis in the detection of 16S rDNA sequence variation in rhizobia and methanotrophs. FEMS Microbiol Ecol 24(3):279–285

  55. von Wintzingerode F, Göbel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21(3):213–229

  56. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

  57. Wang C, Dang H, Ding Y (2008) Incidence of diverse integrons and β-lactamase genes in environmental Enterobacteriaceae isolates from Jiaozhou Bay, China. World J Microbiol Biotechnol 24(12):2889–2896

  58. Wang Y, Sheng H-F, He Y, Wu J-Y, Jiang Y-X, Tam NF-Y, Zhou H-W (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina tags. Appl Environ Microbiol 78(23):8264–8271

  59. Ying J-Y, Zhang L-M, Wei W-X, He J-Z (2013) Effects of land utilization patterns on soil microbial communities in an acid red soil based on DNA and PLFA analyses. J Soils Sediments 13(7):1223–1231

  60. Zeng Y, Zheng T, Li H (2009) Community composition of the marine bacterioplankton in Kongsfjorden (Spitsbergen) as revealed by 16S rRNA gene analysis. Polar Biol 32(10):1447–1460

  61. Zhang W, Ki J-S, Qian P-Y (2008) Microbial diversity in polluted harbor sediments I: bacterial community assessment based on four clone libraries of 16S rDNA. Estuar Coast Shelf Sci 76(3):668–681

  62. Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, Welch DBM, Martiny JBH, Sogin M, Boetius A, Ramette A (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE 6(9):e24570

Download references

Acknowledgments

This work was supported by the China National Science Foundation grant 40821004. We are also indebted to the members of the Ecological Environment Monitoring Station in Jiaozhou Bay for providing measurements of the physicochemical parameters of the sediment.

Author information

Correspondence to Tian Xiao.

Additional information

Responsible editor: John R. Lawrence

Electronic supplementary material

Below is the link to the electronic supplementary material.

Tables S1

(DOCX 24 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Hu, H., Liu, Y. et al. Bacterial composition and spatiotemporal variation in sediments of Jiaozhou Bay, China. J Soils Sediments 15, 732–744 (2015). https://doi.org/10.1007/s11368-014-1045-7

Download citation

Keywords

  • 16S rRNA clone library
  • Diversity
  • Jiaozhou Bay
  • Sediment bacteria
  • Spatiotemporal distribution