Spatial variations of bacterial community composition in sediments of the Jiaozhou Bay, China

Abstract

Spatial variations of sediment microbes pose a great challenge for the estimation of anthropogenic influence on biogeochemical processes, yet remain very unclear in coastal ecosystems. Surface sediments in 9 stations from the eutrophic Jiaozhou Bay, China, were sampled, DNA was extracted within the sediments, and the 16S rDNA was sequenced with the Illumina Hiseq sequencing. Results reveal considerable heterogeneity of sediment bacteria in the Jiaozhou Bay, of which Proteobacteria and Bacteroidetes accounted for over 75%. Bacterial alpha-diversity indices decreased generally from the outside to the inner part of the bay and from the offshore to the nearshore area. Bacterial community structures of S3, S4, S7, and S8 clustered, those of S5, S13, and S14 grouped together, while those of S6 and S10 were distinct from each other and from those of the other stations. Major class Gammaproteobacteria were more abundant at the stations with mesoeutrophic to eutrophic levels (S4, S5, S8, and S10) and less abundant at oligotrophic stations (S6, S13, and S14), while Deltaproteobacteria had an opposite distribution pattern. Overall, bacterial community composition transitioned from being Xanthomonadales-dominant at S4 and S8 to being unidentifed_Gammaproteobacteria-dominant at S5, S6, S13, and S14, while in other stations there were comparable orders. The biogeochemical processes correspondingly changed from being nitrogen cycling-dominant at S4 and S8 to being sulfur cycling-dominant at S5, S6, S13, and S14. The bacterial distribution patterns were especially affected by the factors (dissolved organic phosphorus, DOP) in the overlying seawater due to the habitat status of P-insufficiency in the bay. Both orders Xanthomonadales and Alteromonadales could serve as bioindicators of anthropogenic pollution to different pollution types. At last, divergent distribution patterns of individual bacterial populations in the bay were revealed, the influential environmental gradients were clarified, and the uncertainty of microbes was reduced, helping to predict environmental functions in coastal areas.

This is a preview of subscription content, access via your institution.

References

  1. Aspila K I, Agemian H, Chau A S Y. 1976. A semi-automated method for the determination of inorganic, organic and total phosphate in sediments. Analyst, 101(1200): 187–197.

    Article  Google Scholar 

  2. Aylagas E, Borja Á, Tangherlini M, Dell’Anno A, Corinaldesi C, Michell C T, Irigoien X, Danovaro R, Rodríguez-Ezpeleta N. 2017. A bacterial community-based index to assess the ecological status of estuarine and coastal environments. Marine Pollution Bulletin, 114(2): 679–688.

    Article  Google Scholar 

  3. Azam F, Malfatti F. 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology, 5(10): 782–791.

    Article  Google Scholar 

  4. Bowman J P, McCuaig R D. 2003. Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Applied and Environmental Microbiology, 69(5): 2 463–2 483.

    Article  Google Scholar 

  5. Budhavant K B, Rao P S P, Safai P D, Granat L, Rodhe H. 2014. Chemical composition of the inorganic fraction of cloud-water at a high altitude station in West India. Atmospheric Environment, 88: 59–65.

    Article  Google Scholar 

  6. Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Lozupone C A, Turnbaugh P J, Fierer N, Knight R. 2011. Global patterns of 16s rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America, 108(S1): 4 516–4 522.

    Article  Google Scholar 

  7. Chen H J, Huang S L, Tseng D H. 2004. Aerobic biotransformation of octylphenol polyethoxylate surfactant in soil microcosms. Environmental Technology, 25(2): 201–210.

    Article  Google Scholar 

  8. Chigineva N I, Aleksandrova A V, Tiunov A V. 2009. The addition of labile carbon alters litter fungal communities and decreases litter decomposition rates. Applied Soil Ecology, 42(3): 264–270.

    Article  Google Scholar 

  9. Cleary D F R, Coelho F J R C, Oliveira V, Gomes N C M, Polónia A R M. 2017. Sediment depth and habitat as predictors of the diversity and composition of sediment bacterial communities in an inter-tidal estuarine environment. Marine Ecology, 38(2): e12411.

    Article  Google Scholar 

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

    Article  Google Scholar 

  11. Dang H Y, Chen R P, Wang L, Guo L Z, Chen P P, Tang Z W, Tian F, Li S Z, Klotz M G. 2010a. Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Applied and Environmental Microbiology, 76(21): 7 036–7 047.

    Article  Google Scholar 

  12. Dang H Y, Li J, Chen R P, Wang L, Guo L Z, Zhang Z N, Klotz M G. 2010b. Diversity, abundance, and spatial distribution of sediment ammonia-oxidizing Betaproteobacteria in response to environmental gradients and coastal eutrophication in Jiaozhou Bay, China. Applied and Environmental Microbiology, 76(14): 4 691–4 702.

    Article  Google Scholar 

  13. Dang H Y, Wang C Y, Li J, Li T G, Tian F, Jin W, Ding Y S, Zhang Z N. 2009. Diversity and distribution of sediment NirS-encoding bacterial assemblages in response to environmental gradients in the Eutrophied Jiaozhou Bay, China. Microbial Ecology, 58(1): 161–169.

    Article  Google Scholar 

  14. Dang H Y, Zhang X X, Sun J, Li T G, Zhang Z N, Yang G P. 2008. Diversity and spatial distribution of sediment ammonia-oxidizing crenarchaeota in response to estuarine and environmental gradients in the Changjiang estuary and East China Sea. Microbiology, 154(7): 2 084–2 095.

    Article  Google Scholar 

  15. DeLorenzo S, Bräuer S L, Edgmont C A, Herfort L, Tebo B M, Zuber P. 2012. Ubiquitous dissolved inorganic carbon assimilation by marine bacteria in the Pacific Northwest coastal ocean as determined by stable isotope probing. PLoS One, 7(10): e46695.

    Article  Google Scholar 

  16. DeMaster D J. 1981. The supply and accumulation of silica in the marine environment. Geochimica et Cosmochimica Acta, 45(10): 1 715–1 732.

    Article  Google Scholar 

  17. DeMaster D J. 1991. Measuring biogenic silica in marine sediments and suspended matter. In: Hurd D C, Spencer D W eds. Marine Particles: Analysis and Characterization. AGU, Washington. p.363–367.

    Google Scholar 

  18. Dortch Q, Whitledge T E. 1992. Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Continental Shelf Research, 12(11): 1 293–1 309.

    Article  Google Scholar 

  19. Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996–998.

    Article  Google Scholar 

  20. Fierer N, Bradford M A, Jackson R B. 2007. Toward an ecological classification of soil bacteria. Ecology, 88(6): 1 354–1 364.

    Article  Google Scholar 

  21. Fuhrman J A, Cram J A, Needham D M. 2015. Marine microbial community dynamics and their ecological interpretation. Nature Reviews Microbiology, 13(3): 133–146.

    Article  Google Scholar 

  22. Gutierrez T, Green D H, Nichols P D, Whitman W B, Semple K T, Aitken M D. 2013. Polycyclovorans algicola gen. nov., sp. nov., an aromatic-hydrocarbon-degrading marine bacterium found associated with laboratory cultures of marine phytoplankton. Applied and Environmental Microbiology, 79(1): 205–214.

    Google Scholar 

  23. Hewson I, Fuhrman J A. 2004. Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Applied and Environmental Microbiology, 70(6): 3 425–3 433.

    Article  Google Scholar 

  24. Juhasz A L, Stanley G A, Britz M L. 2000. Microbial degradation and detoxification of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia strain VUN 10, 003. Letters in Applied Microbiology, 30(5): 396–401.

    Article  Google Scholar 

  25. Justić D, Rabalais N N, Turner R E. 1995. Stoichiometric nutrient balance and origin of coastal eutrophication. Marine Pollution Bulletin, 30(1): 41–46.

    Article  Google Scholar 

  26. Kan J J, Suzuki M T, Wang K, Evans S E, Chen F. 2007. High temporal but low spatial heterogeneity of bacterioplankton in the Chesapeake Bay. Applied and Environmental Microbiology, 73(21): 6 776–6 789.

    Article  Google Scholar 

  27. Kanaly R A, Harayama S. 2010. Advances in the field of high-molecular-weight polycyclic aromatic hydrocarbon biodegradation by bacteria. Microbial Biotechnology, 3(2): 136–164.

    Article  Google Scholar 

  28. Kieft B, Li Z, Bryson S, Crump B C, Hettich R, Pan C L, Mayali X, Mueller R S. 2018. Microbial community structure-function relationships in Yaquina Bay estuary reveal spatially distinct carbon and nitrogen cycling capacities. Frontiers in Microbiology, 9: 1 282.

    Article  Google Scholar 

  29. Li K Q, He J, Li J L, Guo Q, Liang S K, Li Y B, Wang X L. 2018. Linking water quality with the total pollutant load control management for nitrogen in Jiaozhou Bay, China. Ecological Indicators, 85: 57–66.

    Article  Google Scholar 

  30. Liu J J, Diao Z H, Xu X R, Xie Q. 2019. Effects of dissolved oxygen, salinity, nitrogen and phosphorus on the release of heavy metals from coastal sediments. Science of the Total Environment, 666: 894–901.

    Article  Google Scholar 

  31. Liu S M, Ye X W, Zhang J, Zhao Y F. 2002. Problems with biogenic silica measurement in marginal seas. Marine Geology, 192(4): 383–392.

    Article  Google Scholar 

  32. Liu X, Hu H W, Liu Y R, Xiao K Q, Cheng F S, Li J, Xiao T. 2015. Bacterial composition and spatiotemporal variation in sediments of Jiaozhou Bay, China. Journal of Soils and Sediments, 15(3): 732–744.

    Article  Google Scholar 

  33. Liu X, Xiao T, Luan Q S, Zhang W Y, Wang M Q, Yue H D. 2011. Bacterial diversity, composition and temporal-spatial variation in the sediment of Jiaozhou Bay, China. Chinese Journal of Oceanology and Limnology, 29(3): 576–590.

    Article  Google Scholar 

  34. Llorens-Marès T, Yooseph S, Goll J, Hoffman J, Vila-Costa M, Borrego C M, Dupont C L, Casamayor E O. 2015. Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics. The ISME Journal, 9(7): 1 648–1 661.

    Article  Google Scholar 

  35. Mortlock R A, Froelich P N. 1989. A simple method for the rapid determination of biogenic opal in pelagic marine sediments. Deep Sea Research Part A. Oceanographic Research Papers, 36(9): 1 415–1 426.

    Article  Google Scholar 

  36. Naghoni A, Emtiazi G, Amoozegar M A, Cretoiu M S, Stal L J, Etemadifar Z, Shahzadeh Fazeli S A, Bolhuis H. 2017. Microbial diversity in the hypersaline Lake Meyghan, Iran. Scientific Reports, 7(1): 11 522.

    Article  Google Scholar 

  37. Nogales B, Lanfranconi M P, Piña-Villalonga J M, Bosch R. 2011. Anthropogenic perturbations in marine microbial communities. FEMS Microbiology Reviews, 35(2): 275–298.

    Article  Google Scholar 

  38. Plugge C M, Zhang W W, Scholten J C M, Stams A J M. 2011. Metabolic flexibility of sulfate-reducing bacteria. Frontiers in Microbiology, 2: 81.

    Article  Google Scholar 

  39. Ravenschlag K, Sahm K, Knoblauch C, Jørgensen B B, Amann R. 2000. Community structure, cellular rRNA content, and activity of sulfate-reducing bacteria in marine arctic sediments. Applied and Environmental Microbiology, 66(8): 3 592–3 602.

    Article  Google Scholar 

  40. Simonin M, Voss K A, Hassett B A, Rocca J D, Wang S Y, Bier R L, Violin C R, Wright J P, Bernhardt E S. 2019. In search of microbial indicator taxa: shifts in stream bacterial communities along an urbanization gradient. Environmental Microbiology, 21(10): 3 653–3 668.

    Article  Google Scholar 

  41. Stieglmeier M, Klingl A, Alves R J E, Rittmann S K M R, Michael M, Leisch N, Schleper C. 2014. Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota. International Journal of Systematic and Evolutionary Microbiology, 64(8): 2 738–2 752.

    Google Scholar 

  42. Su M L, Jing Z, Hong T C, Guo S Z. 2005. Factors influencing nutrient dynamics in the eutrophic Jiaozhou Bay, North China. Progress in Oceanography, 66(1): 66–85.

    Article  Google Scholar 

  43. Sun F L, Wang Y S, Wu M L, Wang Y T, Li Q P. 2011. Spatial heterogeneity of bacterial community structure in the sediments of the Pearl River estuary. Biologgia, 66(4): 574–584.

    Google Scholar 

  44. Suzuki R, Ishimaru T. 1990. An improved method for the determination of phytoplankton chlorophyll using N, N-dimethylformamide. Journal of the Oceanographical Society of Japan, 46(4): 190–194.

    Article  Google Scholar 

  45. Wang H Y, Jiang X L, He Y, Guan H S. 2009. Spatial and seasonal variations in bacterial communities of the Yellow Sea by T-RFLP analysis. Frontiers of Environmental Science & Engineering in China, 3(2): 194–199.

    Article  Google Scholar 

  46. Wang H, He Z L, Lu Z M, Zhou J Z, Van Nostrand J D, Xu X H, Zhang Z J. 2012. Genetic linkage of soil carbon pools and microbial functions in subtropical freshwater wetlands in response to experimental warming. Applied and Environmental Microbiology, 78(21): 7 652–7 661.

    Article  Google Scholar 

  47. Wang Q, Garrity G M, Tiedje J M, Cole J R. 2007. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5 261–5 267.

    Article  Google Scholar 

  48. Xing J W, Song J M, Yuan H M, Li X G, Li N, Duan L Q, Kang X M, Wang Q D. 2017. Fluxes, seasonal patterns and sources of various nutrient species (nitrogen, phosphorus and silicon) in atmospheric wet deposition and their ecological effects on Jiaozhou Bay, North China. Science of the Total Environment, 576: 617–627.

    Article  Google Scholar 

  49. Yokokawa T, Nagata T. 2010. Linking bacterial community structure to carbon fluxes in marine environments. Journal of Oceanography, 66(1): 1–12.

    Article  Google Scholar 

  50. Yu S X, Pang Y L, Wang Y C, Li J L, Qin S. 2018. Distribution of bacterial communities along the spatial and environmental gradients from Bohai Sea to northern Yellow Sea. Peer J, 6: e4272.

    Article  Google Scholar 

  51. Yuan H M, Song J M, Xing J W, Li X G, Li N, Duan L Q, Qu B X, Wang Y D. 2018. Spatial and seasonal variations, partitioning and fluxes of dissolved and particulate nutrients in Jiaozhou Bay. Continental Shelf Research, 171: 140–149.

    Article  Google Scholar 

  52. Yuan Y, Song D H, Wu W, Liang S K, Wang Y, Ren Z P. 2016. The impact of anthropogenic activities on marine environment in Jiaozhou Bay, Qingdao, China: a review and a case study. Regional Studies in Marine Science, 8: 287–296.

    Article  Google Scholar 

  53. Zhang C, Liu G B, Xue S, Wang G L. 2016. Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biology and Biochemistry, 97: 40–49.

    Article  Google Scholar 

Download references

Acknowledgment

The authors thank the crews of R/V Chuangxin for supports in data collection, and Prof. SUN Xiaoxia for support in Chl a data processing.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jinming Song.

Additional information

Supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA23050501) and the Key Special Projects of Marine Science and Technology Funds of Shandong Province and Pilot National Laboratory for Marine Science and Technology (Qingdao) (No. 2018SDKJ0504-1)

Data Availability Statement

The datasets generated during the current study are available from the corresponding author on reasonable request.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sun, Q., Song, J., Li, X. et al. Spatial variations of bacterial community composition in sediments of the Jiaozhou Bay, China. J. Ocean. Limnol. (2021). https://doi.org/10.1007/s00343-020-0127-1

Download citation

Keyword

  • Jiaozhou Bay
  • bacterial community
  • spatial variation
  • sediments
  • overlying water