Skip to main content
SpringerLink
Log in

The Temporal Scaling of Bacterioplankton Composition: High Turnover and Predictability during Shrimp Cultivation

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The spatial distribution of microbial communities has recently been reliably documented in the form of a distance–similarity decay relationship. In contrast, temporal scaling, the pattern defined by the microbial similarity–time relationships (STRs), has received far less attention. As a result, it is unclear whether the spatial and temporal variations of microbial communities share a similar power law. In this study, we applied the 454 pyrosequencing technique to investigate temporal scaling in patterns of bacterioplankton community dynamics during the process of shrimp culture. Our results showed that the similarities decreased significantly (P = 0.002) with time during the period over which the bacterioplankton community was monitored, with a scaling exponent of w = 0.400. However, the diversities did not change dramatically. The community dynamics followed a gradual process of succession relative to the parent communities, with greater similarities between samples from consecutive sampling points. In particular, the variations of the bacterial communities from different ponds shared similar successional trajectories, suggesting that bacterial temporal dynamics are predictable to a certain extent. Changes in bacterial community structure were significantly correlated with the combination of Chl a, TN, PO4 3-, and the C/N ratio. In this study, we identified predictable patterns in the temporal dynamics of bacterioplankton community structure, demonstrating that the STR of the bacterial community mirrors the spatial distance–similarity decay model.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. APHA (1976) Standard methods for the examination of water and wastewater 14ed. APHA American Public Health Association

  3. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows integration and analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Case M, Leca EE, Leitaoc SN, SantAnna EE, Schwamborn R, De Moraes Junior AT (2008) Plankton community as an indicator of water quality in tropical shrimp culture ponds. Mar Pollut Bull 56:1343–1352

    Article  CAS  PubMed  Google Scholar 

  5. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  6. Comte J, Del Giorgio PA (2010) Linking the patterns of change in composition and functional capacities in bacterioplankton successions along environmental gradients. Ecology 95:1466–1476

    Article  Google Scholar 

  7. Comte J, Del Giorgio PA (2011) Composition influences the pathway but not the outcome of the metabolic response of bacterioplankton to resource shifts. PLoS One 6:e25266

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Cotner JB, Biddanda BA (2002) Small players, large role: Microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121

    Article  CAS  Google Scholar 

  9. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM et al (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:394–399

    Article  Google Scholar 

  11. Domingues RB, Barbosa A, Galvão H (2008) Constraints on the use of phytoplankton as a biological quality element within the water framework directive in Portuguese waters. Mar Pollut Bull 56:1389–1395

    Article  CAS  PubMed  Google Scholar 

  12. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  13. Ferreira NC, Bonetti C, Seiffert WQ (2011) Hydrological and water quality indices as management tools in marine shrimp culture. Aquaculture 318:425–433

    Article  Google Scholar 

  14. Fierer N, Nemergut DR, Knight R, Crainej JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642

    Article  PubMed  Google Scholar 

  15. Gilbert JA, Field D, Swift P, Newbold L, Oliver A, Smyth T et al (2009) The seasonal succession of microbial communities in the Western English Channel using 16S rDNA-tag pyrosequencing. Environ Microbiol 11:3132–3139

    Article  CAS  PubMed  Google Scholar 

  16. Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M et al (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750

    Article  CAS  PubMed  Google Scholar 

  17. Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654

    Article  PubMed  Google Scholar 

  18. Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2:1–10

    Google Scholar 

  19. Gómez-Consarnau L, Lindh MV, Gasol JM, Pinhassi J (2012) Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ Microbiol 14:2361–2378

    Article  PubMed  Google Scholar 

  20. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  21. Johnson EA, Miyanishi K (2008) Testing the assumptions of chronosequences in succession. Ecol Lett 11:419–431

    Article  PubMed  Google Scholar 

  22. Jones SE, Cadkin TA, Newton RJ, McMahon KD (2012) Spatial and temporal scales of aquatic bacterial beta diversity. Front Microbiol 3:318

    PubMed Central  PubMed  Google Scholar 

  23. Kim Y, Jeong J, Wells GF, Park H (2013) General and rare bacterial taxa demonstrating different temporal dynamic patterns in an activated sludge bioreactor. Appl Microbiol Biotechnol 97:1755–1765

    Article  CAS  PubMed  Google Scholar 

  24. Lemonnier H, Herbland A, Salery L, Soulard B (2006) “Summer syndrome” in Litopenaeus stylirostris grow out ponds in New Caledonia: zootechnical and environmental factors. Aquaculture 261:1039–1047

    Article  Google Scholar 

  25. Lemonnier H, Courties C, Mugnier C, Torréton J, Herbland A (2010) Nutrient and microbial dynamics in eutrophying shrimp ponds affected or unaffected by vibriosis. Mar Pollut Bull 60:402–411

    Article  CAS  PubMed  Google Scholar 

  26. Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn. Developments in environmental modeling. Dev Environ Model 20:1–853

    Google Scholar 

  27. Lucas R, Courties C, Herbland A, Goulletquer P, Marteau AL, Lemonnier H (2010) Etrophication in a tropical pond: understanding the bacterioplankton and phytoplankton dynamics during a vibriosis outbreak using flow cytometric analyses. Aquaculture 310:112–121

    Article  Google Scholar 

  28. Lundin D, Severin I, Logue JB, Östman Ö, Andersson AF, Lindström ES (2012) Which sequencing depth is sufficient to describe patterns in bacterial α- and β-diversity? Environ Microbiol Rep 4:367–372

    Article  CAS  PubMed  Google Scholar 

  29. Ma Z, Song X, Wan R, Gao L (2013) A modified water quality index for intensive shrimp ponds of Litopenaeus vannamei. Ecol Indic 24:287–293

    Article  CAS  Google Scholar 

  30. Or A, Shtrasler L, Gophna U (2012) Fine-scale temporal dynamics of a fragmented lotic microbial ecosystem. Sci Rep 2:207

    Article  PubMed Central  PubMed  Google Scholar 

  31. Paver SF, Hayek KR, Gano KA, Fagen JR, Brown CT et al (2013) Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. Environ Microbiol 15:2489–2504

    Article  PubMed  Google Scholar 

  32. Preston FW (1960) Time and space and the variation of species. Ecology 41:612–627

    Article  Google Scholar 

  33. R Development Team (2012) R: A language and environment for statistical computing. http://cran.r-project.org

  34. Redford A, Fierer N (2009) Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb Ecol 58:189–198

    Article  PubMed  Google Scholar 

  35. Shade A, Caporaso JG, Handelsman J, Knight R, Fierer N (2013) A meta-analysis of changes in bacterial and archaeal communities with time. ISME J 7:1493–1506

    Article  PubMed Central  PubMed  Google Scholar 

  36. Sørensen TA (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species and its application to analyses of the vegetation on Danish commons. Biol Skr 5:1–34

    Google Scholar 

  37. Snieszko SF (1974) The effect of environmental stress on outbreaks of infectious diseases of fish. J Fish Biol 6:197–208

    Article  Google Scholar 

  38. Sung H, Hsu S, Chen C, Ting Y, Chao W (2001) Relationships between disease outbreak in cultured tiger shrimp (Penaeus monodon) and the composition of Vibrio communities in pond water and shrimp hepatopancreas during cultivation. Aquaculture 192:101–110

    Article  Google Scholar 

  39. Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM et al (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611

    Article  CAS  PubMed  Google Scholar 

  40. Van Der Gast CJ, Ager D, Lilley AK (2008) Temporal scaling of bacterial taxa is influenced by both stochastic and deterministic ecological factors. Environ Microbiol 10:1411–1418

    Article  PubMed  Google Scholar 

  41. Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC et al (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Wells GF, Park HD, Eggleston B, Francis CA, Criddle CS (2011) Fine-scale bacterial community dynamics and the taxa–time relationship within a full-scale activated sludge bioreactor. Water Res 45:5476–5488

    Article  CAS  PubMed  Google Scholar 

  43. White EP, Adler PB, Lauenroth WK, Gill RA, Greenberg D et al (2006) A comparison of the species–time relationship across ecosystems and taxonomic groups. Oikos 112:185–195

    Article  Google Scholar 

  44. Wu QL, Hahn MW (2006) High predictability of the seasonal dynamics of a species-like Polynucleobacter population in a freshwater lake. Environ Microbiol 8:1660–1666

    Article  CAS  PubMed  Google Scholar 

  45. Xiong J, Wu L, Tu S, Van Nostrand JD, He Z, Zhou J, Wang G (2010) Microbial communities and functional genes associated with soil arsenic contamination and rhizosphere of the arsenic hyper-accumulating plant Pteris vittata L. Appl Environ Microbiol 76:7277–7284

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Xiong J, He Z, Van Nostrand JD, Luo G, Tu S, Zhou J, Wang G (2012) Assessing the microbial community and functional genes in a vertical soil profile with long-term arsenic contamination. PLoS One 7:e50507

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J et al (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Xu H, Zhu M, Jiang Y, Al-Rasheid KS (2010) Temporal species distributions of planktonic protist communities in semi-enclosed mariculture waters and responses to environmental stress. Acta Oceanol Sin 29:74–83

    Article  Google Scholar 

  49. Zhang D, Wang X, Xiong J, Zhu J, Wang Y, Zhao Q et al (2013) Bacterioplankton assemblages as biological indicators for shrimp healthy states. Ecol Indic. doi:10.1016/j.ecolind.2013.11.002

    Google Scholar 

  50. Zhou J, Liu W, Deng Y, Jiang Y, Xue K, He s et al (2013) Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community. mBio 4:e00584–12

    PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National High Technology Research and Development Program of China (863 Program, 2012AA092000), the Science and Technology Project of the Ministry of Education (Grant No. 208053), the Natural Science Foundation of Ningbo City (2013A610169), the Research Fund from 2011 Center of Modern Marine Aquaculture of East China Sea, and the KC Wong Magna Fund of Ningbo University.

Author information

Authors and Affiliations

  1. Faculty of Marine Sciences, Ningbo University, Ningbo, 315211, China

    Jinbo Xiong, Kai Wang, Qunfen Zhao, Manhua Hou, Linglin Qiuqian & Demin Zhang

  2. Faculty of Architectural, Civil Engineering and Environment, Ningbo University, Ningbo, 315211, China

    Jianlin Zhu

  3. Medical School, Ningbo University, Ningbo, 315211, China

    Xin Wang

  4. 2011 Center of Modern Marine Aquaculture of East China Sea, Ningbo, China

    Jinbo Xiong, Kai Wang & Demin Zhang

  5. Marine Environmental Monitoring Center of Ningbo, SOA, Ningbo, 315012, China

    Xiansen Ye & Lian Liu

Authors
  1. Jinbo Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianlin Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiansen Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qunfen Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Manhua Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Linglin Qiuqian
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Demin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Demin Zhang.

Additional information

Xiong and Zhu contributed equally to this work

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOC 72 kb)

Table S2

(DOC 47 kb)

Fig. S1

(DOC 135 kb)

Fig. S2

(DOC 151 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xiong, J., Zhu, J., Wang, K. et al. The Temporal Scaling of Bacterioplankton Composition: High Turnover and Predictability during Shrimp Cultivation. Microb Ecol 67, 256–264 (2014). https://doi.org/10.1007/s00248-013-0336-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0336-7

Keywords

Search

Navigation