Skip to main content

Advertisement

Log in

Metaproteomic analysis of bacterial communities in marine mudflat aquaculture sediment

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Bacteria living in marine sediment play crucial roles in the benthic–pelagic interface coupling process. However, the complexity of the marine environment and the abundance of interfering materials hamper metaproteomic research of the marine mudflat environment. In this study, a modified sequential protein extraction method was used for marine mudflat sediment metaproteomic investigation. For marine sediment samples in cultured clam mudflat, more than 1000 protein spots were visualized in a two-dimensional gel electrophoresis map and 78 % of 194 randomly selected spots were successfully identified by mass spectrometry. We further applied this method to compare long-term clam aquaculture and natural mudflat sediment and identified 53 altered proteins from different microbe resources, which belonged to different functional categories or metabolic pathways. We found that proteins involved in stress/defense response process, ATP regeneration and protein folding more inclined to increase abundance while arginine biosynthesis and signal transduction process related proteins preferred to decrease in clam cultured mudflat sediment. Meanwhile, proteins were abundant in pathogens of bivalves, such as Vibrio and Photobacterium, and decreased in Acinetobacter, after about 8 months clam cultured. Furthermore, the terminal restriction fragment length polymorphism assay was performed to compare microbial community composition between sediments mentioned above. Results showed that the top three enrich genera in natural sediment were Cytophaga, Butyrivibrio and Spirochaeta, while Cytophaga, Spirochaeta and Azoarcus were found enrichment in long-term mudflat aquaculture sediment.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abram F, Gunnigle E, O’Flaherty V (2009) Optimisation of protein extraction and 2-DE for metaproteomics of microbial communities from anaerobic wastewater treatment biofilms. Electrophoresis 30(23):4149–4151. doi:10.1002/elps.200900474

    Article  CAS  Google Scholar 

  • Bowen JL, Ward BB, Morrison HG, Hobbie JE, Valiela I, Deegan LA, Sogin ML (2011) Microbial community composition in sediments resists perturbation by nutrient enrichment. ISME J 5(9):1540–1548. doi:10.1038/ismej.2011.22

    Article  Google Scholar 

  • Chen S, Rillig MC, Wang W (2009) Improving soil protein extraction for metaproteome analysis and glomalin-related soil protein detection. Proteomics 9(21):4970–4973

    Article  CAS  Google Scholar 

  • Chourey K, Jansson J, VerBerkmoes N, Shah M, Chavarria KL, Tom LM, Brodie EL, Hettich RL (2010) Direct cellular lysis/protein extraction protocol for soil metaproteomics. J Proteome Res 9(12):6615–6622

    Article  CAS  Google Scholar 

  • Du J, Xiao K, Huang Y, Li H, Tan H, Cao L, Lu Y, Zhou S (2011) Seasonal and spatial diversity of microbial communities in marine sediments of the South China Sea. Antonie Van Leeuwenhoek 100(3):317–331. doi:10.1007/s10482-011-9587-9

    Article  Google Scholar 

  • Erickson BK, Mueller RS, VerBerkmoes NC, Shah M, Singer SW, Thelen MP, Banfield JF, Hettich RL (2010) Computational prediction and experimental validation of signal peptide cleavages in the extracellular proteome of a natural microbial community. J Proteome Res 9(5):2148–2159. doi:10.1021/pr900877a

    Article  CAS  Google Scholar 

  • Fang C, Zhuang Y, Xu T, Li Y, Li Y, Lin W (2013) Changes in rice allelopathy and rhizosphere microflora by inhibiting rice phenylalanine ammonia-lyase gene expression. J Chem Ecol 39(2):204–212. doi:10.1007/s10886-013-0249-4

    Article  CAS  Google Scholar 

  • Findlay RH, Watling L (1998) Seasonal variation in the structure of a marine benthic microbial community. Microb Ecol 36(1):23–30

    Article  Google Scholar 

  • Findlay RH, Trexler MB, Guckert J, White DC (1990) Laboratory study of disturbance in marine sediments: response of a microbial community. Mar Ecol Prog Ser Oldend 62(1):121–133

    Article  Google Scholar 

  • Georges AA, El-Swais H, Craig SE, Li WK, Walsh DA (2014) Metaproteomic analysis of a winter to spring succession in coastal northwest Atlantic Ocean microbial plankton. ISME J 8(6):1301–1313. doi:10.1038/ismej.2013.234

    Article  CAS  Google Scholar 

  • Gray JS (2002) Biomagnification in marine systems: the perspective of an ecologist. Mar Pollut Bull 45(1–12):46–52

    Article  CAS  Google Scholar 

  • Jarosz DF, Lindquist S (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330(6012):1820–1824. doi:10.1126/science.1195487

    Article  CAS  Google Scholar 

  • Karthik M, Suri J, Saharan N, Biradar R (2005) Brackish water aquaculture site selection in Palghar Taluk, Thane district of Maharashtra, India, using the techniques of remote sensing and geographical information system. Aquacult Eng 32(2):285–302

    Article  Google Scholar 

  • Kavaliauskas D, Nissen P, Knudsen CR (2012) The busiest of all ribosomal assistants: elongation factor Tu. Biochemistry 51(13):2642–2651

    Article  CAS  Google Scholar 

  • Kleiner M, Wentrup C, Lott C, Teeling H, Wetzel S, Young J, Chang YJ, Shah M, VerBerkmoes NC, Zarzycki J, Fuchs G, Markert S, Hempel K, Voigt B, Becher D, Liebeke M, Lalk M, Albrecht D, Hecker M, Schweder T, Dubilier N (2012) Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. Proc Natl Acad Sci USA 109(19):E1173–E1182. doi:10.1073/pnas.1121198109

    Article  CAS  Google Scholar 

  • Lin X, Cook TJ, Zabetian CP, Leverenz JB, Peskind ER, Hu S-C, Cain KC, Pan C, Edgar JS, Goodlett DR, Racette BA, Checkoway H, Montine TJ, Shi M, Zhang J (2012a) DJ-1 isoforms in whole blood as potential biomarkers of Parkinson disease. Sci Rep 2:954. http://www.nature.com/srep/2012/121211/srep00954/abs/srep00954.html#supplementary-information

  • Lin XM, Wang C, Guo C, Tian YM, Li H, Peng XX (2012b) Differential regulation of OmpC and OmpF by AtpB in Escherichia coli exposed to nalidixic acid and chlortetracycline. J Proteomics 75(18):5898–5910

    Article  CAS  Google Scholar 

  • Liu X, Gao H, Xiao N, Liu Y, Li J, Li L (2015) Outer membrane protein U (OmpU) mediates adhesion of Vibrio mimicus to host cells via two novel N-terminal motifs. PLoS ONE 10(3):e0119026. doi:10.1371/journal.pone.0119026

    Article  Google Scholar 

  • Lomstein BA, Langerhuus AT, D’Hondt S, Jorgensen BB, Spivack AJ (2012) Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484(7392):101–104. doi:10.1038/nature10905

    Article  CAS  Google Scholar 

  • Maron P-A, Ranjard L, Mougel C, Lemanceau P (2007) Metaproteomics: a new approach for studying functional microbial ecology. Microb Ecol 53(3):486–493

    Article  CAS  Google Scholar 

  • Narayanasamy S, Muller EE, Sheik AR, Wilmes P (2015) Integrated omics for the identification of key functionalities in biological wastewater treatment microbial communities. Microb Biotechnol. doi:10.1111/1751-7915.12255

    Google Scholar 

  • Pierre-Alain M, Christophe M, Severine S, Houria A, Philippe L, Lionel R (2007) Protein extraction and fingerprinting optimization of bacterial communities in natural environment. Microb Ecol 53(3):426–434. doi:10.1007/s00248-006-9121-1

    Article  CAS  Google Scholar 

  • Qureshi ZA, Hittle LE, O’Hara JA, Rivera JI, Syed A, Shields RK, Pasculle AW, Ernst RK, Doi Y (2015) Colistin-resistant Acinetobacter baumannii: beyond carbapenem resistance. Clin Infect Dis. doi:10.1093/cid/civ048

    Google Scholar 

  • Ramos-Gonzalez MI, Ben-Bassat A, Campos MJ, Ramos JL (2003) Genetic engineering of a highly solvent-tolerant Pseudomonas putida strain for biotransformation of toluene to p-hydroxybenzoate. Appl Environ Microbiol 69(9):5120–5127

    Article  CAS  Google Scholar 

  • Selby K, Lindstrom M, Somervuo P, Heap JT, Minton NP, Korkeala H (2011) Important role of class I heat shock genes hrcA and dnaK in the heat shock response and the response to pH and NaCl stress of group I Clostridium botulinum strain ATCC 3502. Appl Environ Microbiol 77(9):2823–2830. doi:10.1128/AEM.02633-10

    Article  CAS  Google Scholar 

  • Siggins A, Gunnigle E, Abram F (2012) Exploring mixed microbial community functioning: recent advances in metaproteomics. FEMS Microbiol Ecol 80(2):265–280. doi:10.1111/j.1574-6941.2011.01284.x

    Article  CAS  Google Scholar 

  • Sowell SM, Wilhelm LJ, Norbeck AD, Lipton MS, Nicora CD, Barofsky DF, Carlson CA, Smith RD, Giovanonni SJ (2009) Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J 3(1):93–105. doi:10.1038/ismej.2008.83

    Article  CAS  Google Scholar 

  • Stokke R, Roalkvam I, Lanzen A, Haflidason H, Steen IH (2012) Integrated metagenomic and metaproteomic analyses of an ANME-1-dominated community in marine cold seep sediments. Environ Microbiol 14(5):1333–1346. doi:10.1111/j.1462-2920.2012.02716.x

    Article  CAS  Google Scholar 

  • Tamber S, Hancock RE (2006) Involvement of two related porins, OprD and OpdP, in the uptake of arginine by Pseudomonas aeruginosa. FEMS Microbiol Lett 260(1):23–29. doi:10.1111/j.1574-6968.2006.00293.x

    Article  CAS  Google Scholar 

  • Tamber S, Ochs MM, Hancock RE (2006) Role of the novel OprD family of porins in nutrient uptake in Pseudomonas aeruginosa. J Bacteriol 188(1):45–54. doi:10.1128/JB.188.1.45-54.2006

    Article  CAS  Google Scholar 

  • Vandieken V, Thamdrup B (2013) Identification of acetate-oxidizing bacteria in a coastal marine surface sediment by RNA-stable isotope probing in anoxic slurries and intact cores. FEMS Microbiol Ecol 84(2):373–386. doi:10.1111/1574-6941.12069

    Article  CAS  Google Scholar 

  • VerBerkmoes NC, Denef VJ, Hettich RL, Banfield JF (2009) Systems biology: functional analysis of natural microbial consortia using community proteomics. Nat Rev Microbiol 7(3):196–205

    Article  CAS  Google Scholar 

  • Wang F, Wall G (2010) Mudflat development in Jiangsu Province, China: practices and experiences. Ocean Coast Manag 53(11):691–699

    Article  Google Scholar 

  • Wang G, Xie J, Yin G, Yu D, Yu E, Wang H, Gong W (2010) Influences of aquiculture on ecological environment. Int J Biol 2(2):158–164

    Article  Google Scholar 

  • Wang HB, Zhang ZX, Li H, He HB, Fang CX, Zhang AJ, Li QS, Chen RS, Guo XK, Lin HF, Wu LK, Lin S, Chen T, Lin RY, Peng XX, Lin WX (2011a) Characterization of metaproteomics in crop rhizospheric soil. J Proteome Res 10(3):932–940. doi:10.1021/pr100981r

    Article  CAS  Google Scholar 

  • Wang Q, Chen J, Liu R, Jia J (2011b) Identification and evaluation of an outer membrane protein OmpU from a pathogenic Vibrio harveyi isolate as vaccine candidate in turbot (Scophthalmus maximus). Lett Appl Microbiol 53(1):22–29. doi:10.1111/j.1472-765X.2011.03062.x

    Article  CAS  Google Scholar 

  • Wu L, Wang H, Zhang Z, Lin R, Lin W (2011) Comparative metaproteomic analysis on consecutively Rehmannia glutinosa-monocultured rhizosphere soil. PLoS ONE 6(5):e20611. doi:10.1371/journal.pone.0020611PONE-D-11-02860

    Article  CAS  Google Scholar 

  • Yue X, Liu B, Xiang J, Jia J (2010) Identification and characterization of the pathogenic effect of a Vibrio parahaemolyticus-related bacterium isolated from clam Meretrix meretrix with mass mortality. J Invertebr Pathol 103(2):109–115

    Article  Google Scholar 

  • Zingaro KA, Papoutsakis ET (2012) Toward a semisynthetic stress response system to engineer microbial solvent tolerance. MBio 3(5):e00308-12. doi:10.1128/mBio.00308-12

    Article  Google Scholar 

Download references

Acknowledgments

This work was sponsored by the National Natural Science Foundation of China (No. 31200105 41276133, 31470238 and J1210050), the Fujian Agricultural and Forestry University Foundation for Distinguished Young Scholars (No. XJQ201201), the Fundamental Research Funds for the Central Universities (CXB2011020) and the Special Research Foundation for Public Welfare Marine Program (No. 201005012).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Wenjing Zhang or Wenxiong Lin.

Ethics declarations

Conflict of interest

The authors have declared that no competing interests exist.

Additional information

Rui Lin and Xiangmin Lin have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1138 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, R., Lin, X., Guo, T. et al. Metaproteomic analysis of bacterial communities in marine mudflat aquaculture sediment. World J Microbiol Biotechnol 31, 1397–1408 (2015). https://doi.org/10.1007/s11274-015-1891-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-015-1891-5

Keywords

Navigation