Skip to main content
SpringerLink
Log in

The ecological roles of bacterial populations in the surface sediments of coastal lagoon environments in Japan as revealed by quantification and qualification of 16S rDNA

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

Abstract

Based on quantification and qualification of bacterial 16S rDNA, we verified the bacterial ecological characteristics of surface sediments of Lakes Shinji and Nakaumi, which are representative of coastal lagoons in Japan. Quantification and qualification of the 16S rDNA sequences was carried out using real time polymerase chain reaction and polymerase chain reaction denaturing gradient gel electrophoresis and non-metric multidimensional scaling, respectively. The results revealed that the copy number per gram of sediment ranged from 8.33 × 108 (Lake Nakaumi) to 1.69 × 1011 (Honjo area), suggesting that bacterial carbon contributed only 0.05–9.64 % of the total carbon content in the samples. Compared with other aquatic environments, these results indicate that sedimentary bacteria are not likely to be important transporters of nutrients to higher trophic levels, or to act as carbon sinks in the lagoons. The bacterial compositions of Lake Shinji and Lake Nakaumi and the Honjo area were primarily influenced by sediment grain sizes and salinity, respectively. Statistical comparisons of the environmental properties suggested that the areas that were oxygen-abundant (Lake Shinji) and at a higher temperature (Honjo area) presented efficient organic matter degradation. The 16S rDNA copy number per gram of carbon and nitrogen showed the same tendency. Consequently, the primary roles of bacteria were degradation and preservation of organic materials, and this was affected by oxygen and temperature. These roles were supported by the bacterial diversity rather than the differences in the community compositions of the sedimentary bacteria in these coastal lagoons.

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
Fig. 7

Similar content being viewed by others

References

  • Akoumianaki I, Nomaki H, Pachiadaki M, Kormas KA, Kitazato H, Tokuyama (2012) Low bacterial diversity and high labile organic matter concentrations in the sediments of the Medee deep-sea hypersaline anoxic basin. Microbes Environ 27:504–508

  • Alongi DM (1988) Bacterial productivity and microbial biomass in tropical mangrove sediments. Microb Ecol 15:59–79

    Article  Google Scholar 

  • Alongi DM (1994) The role of bacteria in nutrient recycling in tropical mangrove and other coastal benthic ecosystems. Hydrobiol 285:19–32

    Article  CAS  Google Scholar 

  • Armed F, Bibi MH, Seto K, Ishiga H, Fukushima T, Roser BP (2009) Abundances, distribution, and sources of trace metals in Nakaumi-Honjo coastal lagoon sediments, Japan. Environ Monit Assess 167:473–491

    Google Scholar 

  • Armed F, Bibi MH, Fukushima T, Seto K, Ishiga H (2010) Recent sedimentary environment of coastal lagoon in southwestern Japan: evidence from major and trace elements. Environ Monit Assess 173:167–180

    Google Scholar 

  • Arnosti C, Jørgensen BB, Sagemann J, Thamdrup B (1998) Temperature dependence of microbial degradation of organic matter in marine sediments: polysaccharide hydrolysis, oxygen consumption, and sulfate reduction. Mar Ecol Prog Ser 165:59–70

    Article  CAS  Google Scholar 

  • Barnes RSK (1994) A critical appraisal of the application of Guelorget and Perthuisot’s concepts of the paralic ecosystem and confinement to macrotidal Europe. Estuar Coast Shelf Sci 38:41–48

    Article  Google Scholar 

  • Billen G (1982) Modelling the processes of organic matter degradation and nutrients recycling in sedimentary systems. In: Nedwell DB, Brown CM (eds) Sediment microbiology. Academic Press, New York, USA, pp 15–52

    Google Scholar 

  • Borch NH, Kirchman DL (1999) Protection of protein from bacterial degradation by submicron particles. Aquat Microb Ecol 16:265–272

    Article  Google Scholar 

  • Bouillon S, Moens T, Koedam N, Dahdouh-Guebas F, Baeyens W, Dehairs F (2004) Variability in the origin of carbon substrates for bacterial communities in mangrove sediments. FEMS Microbiol Ecol 49:171–179

    Article  CAS  Google Scholar 

  • Bourgeois S, Pruski AM, Sun MY, Buscail R, Lantoine F, Vétion G, Rivière B, Charles F (2011) Distribution and lability of land-derived organic matter in the surface sediments of the Rhône prodelta and the adjacent shelf (Mediterranean sea, France): a multi proxy study. Biogeosci Discuss 8:3353–3402

    Article  Google Scholar 

  • Boutton TW (1991) Stable carbon isotope ratios of natural materials: II, Atmospheric, terrestrial, marine, and freshwater environments. In: Coleman DC, Fry B (eds) Carbon isotopes techniques. Academic Press, SanDiego, pp 173–185

    Chapter  Google Scholar 

  • Bowen JL, Crump BC, Deegan LA, Hobbie JE (2009) Salt marsh sediment bacteria: their distribution and response to external nutrient inputs. ISME J 3:924–934

    Article  CAS  Google Scholar 

  • Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108:14288–14293

    Article  CAS  Google Scholar 

  • Cho BC, Azam F (1988) Major role of bacteria in biogeochemical fluxes in the ocean’s interior. Nature 332:441–443

    Article  CAS  Google Scholar 

  • Cullen DW, Hirsch PR (1998) Simple and rapid method for direct extraction of microbial DNA from soil for PCR. Soil Biol Biochem 30:983–993

    Article  CAS  Google Scholar 

  • Dale NG (1974) Bacteria in intertidal sediments: factors related to their distribution. Limnol Oceanogr 19:509–518

    Article  Google Scholar 

  • Dang H, Li J, Chen M, Li T, Zeng Z, Yin X (2009) 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 25:179–188

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Danovaro R, Marrale D, Della Croce N, Dell’Anno A, Fabiano M (1998) Heterotrophic nanoflagellates, bacteria and labile organic compounds in continental shelf and deep-sea sediments of the Eastern Mediterranean. Microb Ecol 35:244–255

    Article  CAS  Google Scholar 

  • Dell’Anno A, Bompadre S, Danovaro R (2002) Quantification, base composition, and fate of extracellular DNA in marine sediments. Limnol Oceanogr 47:899–905

    Article  Google Scholar 

  • Deming JW, Barros JA (1993) The early diagenesis of organic matter: bacterial activity. In: Engel MH, Macko SA (eds) Organic geochemistry: principles and applications. Plenum Press, New York, pp 119–144

    Chapter  Google Scholar 

  • Divya B, Parvathi A, Bharathi PAL, Nair S (2011) 16S rRNA-based bacterial diversity in the organic-rich sediments underlying oxygen-deficient waters of the eastern Arabian Sea. World J Microbiol Biotechnol 27:2821–2833

    Article  CAS  Google Scholar 

  • Fabiano M, Danovaro R (1998) Enzymatic activity, bacterial distribution, and organic matter composition in sediments of the Ross Sea (Antarctica). Appl Environ Microbiol 64:3838–3845

    CAS  Google Scholar 

  • Fenchel T, Blackburn TH (1979) Bacteria and mineral cycling. Academic Press, London

    Google Scholar 

  • Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ (2010) Temperature-controlled organic carbon mineralization in lake sediments. Nature 466:478–482

    Article  CAS  Google Scholar 

  • Hartnett HE, Keil RG, Hedges JI, Devol AH (1998) Influence of oxygen exposure time on organic carbon preservation in continental margin sediments. Nature 391:572–575

    Article  CAS  Google Scholar 

  • Harvey HR, Tuttle JH, Bell JT (1995) Kinetics of phytoplankton decay during simulated sedimentation: changes in biochemical composition and microbial activity under oxic and anoxic conditions. Geochim Cosmochim Acta 59:3367–3377

    Article  CAS  Google Scholar 

  • Hashitani H, Okumura M, Fujinaga K, Kondo K, Seike Y (1992) Effect of meteorological factors on the water quality of Lake Shinji and Lake Nakaumi: part 2. Studies San’in Region 8:69–86 (in Japanese, with English Abstract)

    Google Scholar 

  • Hedges JI, Keil RG (1995) Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar Chem 49:81–115

    Article  CAS  Google Scholar 

  • Huang S, Chen C, Wu Y, Wu Q, Zhang R (2011) Characterization of depth-related bacterial communities and their relationships with the environmental factors in the river sediments. World J Microbiol Biotechnol 27:2655–2664

    Article  CAS  Google Scholar 

  • Ichikawa T, Aizaki M, Takeshita M (2007) Numerical study on amelioration of water quality in Lakes Shinji and Nakaumi: a coastal brackish lagoon system. Limnol 8:281–294

    Article  CAS  Google Scholar 

  • Ishitobi Y, Hiratsuka J, Kuwabara H, Yamamuro M (2000) Comparison of fish fauna in three areas of adjacent eutrophic estuarine lagoons with different salinities. J Mar Sys 26:171–181

    Article  Google Scholar 

  • Kabir S, Rajendran N, Amemiya T, Itoh K (2003) Real-time quantitative PCR assay on bacterial DNA: in a model soil system and environmental samples. J Gen Appl Microbiol 49:101–109

    Article  CAS  Google Scholar 

  • Kang KS, Itoh K, Murabayashi M, Nakanishi J (2001) Direct DNA extraction from soil and DNA purification: comparison of the different methods. J Jpn Soc Water Envir 24:175–179 (in Japanese)

    Article  CAS  Google Scholar 

  • Keil RG, Montluçon DB, Prahl FG, Hedges JI (1994) Sorptive preservation of labile organic matter in marine sediments. Nature 370:549–552

    Article  Google Scholar 

  • Kemp PF (1990) The fate of benthic bacterial production. Review Aquat Sci 2:109–124

    Google Scholar 

  • Klappenbach JL, Saxman PR, Cole JR, Schmidt TM (2001) rrdb: the ribosomal RNA operon copy number database. Nucleic Acids Res 29:181–184

    Article  CAS  Google Scholar 

  • Knoppers B (1994) Aquatic primary production in coastal lagoons. In: Kjerfve B (ed) Coastal lagoon processes. Elsevier Science Publishers, Amsterdam, pp 243–286

    Chapter  Google Scholar 

  • Kormas KA (2011) Interpreting diversity of Proteobacteria based on 16S rRNA gene copy number. In: Sezenna ML (ed) Proteobacteria: phylogeny, metabolic diversity and ecological effects. Nova Publishers, Hauppauge, New York, pp 73–89

    Google Scholar 

  • Kormas KA, Papaspyrou S (2004) Growth of marine bacterioplankton on river and sea water dissolved organic carbon in a Mediterranean coastal system. Cah Biol Mar 45:55–64

    Google Scholar 

  • Leloup J, Loy A, Knab NJ, Borowski C, Wagner M, Jørgensen BB (2007) Diversity and abundance of sulfate-reducing microorganisms in the sulfate and methane zones of a marine sediment, Black Sea. Environ Microbiol 9:131–142

    Article  CAS  Google Scholar 

  • Manini E, Fiordelmondo C, Gambi C, Puscddu A, Danovaro R (2003) Benthic microbial loop functioning in coastal lagoons: a comparative approach. Oceanol Acta 26:27–38

    Article  CAS  Google Scholar 

  • Mayer LM (1989) Extracellular proteolytic enzyme activity in sediments of an intertidal mudflat. Limnol Oceanogr 34:973–981

    Article  CAS  Google Scholar 

  • Middelburg JJ, Nieuwenhuize J (1998) Carbon and nitrogen isotopes in suspended matter and sediments from the Schelde Estuary. Mar Chem 60:217–225

    Article  CAS  Google Scholar 

  • Müller AK, Westergaard K, Christensen S, Sørensen SJ (2001) The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol Ecol 36:11–19

    Article  Google Scholar 

  • Muyzer G, de waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH (2007) Vegan: community ecology package. R package version 1.8-8

  • Owens NJP (1987) Natural variations in 15 N in the marine environment. Adv Mar Biol 24:389–451

    Article  Google Scholar 

  • Pastor L, Deflandre B, Viollier E, Cathalot C, Metzger E, Rabouille C, Escoubeyrou K, Lloret E, Pruski AM, Vétion G, Desmalades M, Buscail R, Grémare A (2011) Influence of the organic matter composition on benthic oxygen demand in the Rhône River prodelta (NW Mediterranean Sea). Cont Shelf Res 31:1008–1019

    Article  Google Scholar 

  • Payne JW (1980) Transport and utilization of peptides by bacteria. In: Payne JW (ed) Microorganisms and nitrogen sources: transport and utilization of amino acids, peptides, proteins, and related substrates. Wiley, New York, pp 212–256

    Google Scholar 

  • Pedersen TF (1995) Sedimentary organic matter preservation: an assessment and speculative synthesis—a comment. Mar Chem 49:117–119

    Article  CAS  Google Scholar 

  • Pei AY, Oberdorf WE, Nossa CW et al (2010) Diversity of 16S rRNA genes within individual prokaryotic genomes. Appl Environ Microbiol 76:3886–3897

    Article  CAS  Google Scholar 

  • Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14:993–1008

    Article  CAS  Google Scholar 

  • Powell SM, Bowman JP, Snape I, Stark JS (2003) Microbial community variation in pristine and polluted nearshore Antarctic sediments. FEMS Microbiol Ecol 45:135–145

    Article  CAS  Google Scholar 

  • Pusceddu A, Sarà G, Armeni M, Fabiano M, Mazzola A (1999) Seasonal and spatial changes in the sediment organic matter of a semienclosed marine system (W-Mediterranean Sea). Hydrobiol 397:59–70

    Article  CAS  Google Scholar 

  • Rajendran N, Matsuda O, Urushigawa Y, Simidu U (1994) Characterization of microbial community structure in the surface sediment of Osaka Bay, Japan, by phospholipid fatty acid analysis. Appl Environ Microbiol 60:248–257

    CAS  Google Scholar 

  • Rublee PA (1982) Seasonal distribution of bacteria in salt marsh sediments in North Carolina. Estuar Coast Shelf Sci 15:67–74

    Article  Google Scholar 

  • Schippers A, Neretin LN, Kallmeyer J, Ferdelman TG, Cragg BA, Parkes RJ, Jørgensen BB (2005) Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433:861–864

    Article  CAS  Google Scholar 

  • Schwarz JI, Eckert W, Conrad R (2007) Community structure of Archaea and Bacteria in a profundal lake sediment Lake Kinneret (Israel). Syst Appl Microbiol 30:239–254

    Article  CAS  Google Scholar 

  • Schweitzer B, Huber I, Amann R, Ludwig W, Simon M (2001) α- and β- proteobacteria control the consumption and release of amino acids on lake snow aggregates. Appl Environ Microbiol 67:632–645

    Article  CAS  Google Scholar 

  • Schwinghamer P, Tan FC, Gordon DC Jr (1983) Stable carbon isotope studies on the Pecks cove mudflat ecosystem in the Cumberland Basin, Bay of Fundy. Can J Fish Aquat Sci 40(suppl 1):262–272

    Article  Google Scholar 

  • Seto K, Nakayama D, Tanaka H, Yamaguchi K (2000) Cyanobacterial water—bloom in Lake Shinji and its geochemical features. LAGUNA 7:61–69 (in Japanese, with English Abstract)

    Google Scholar 

  • Somura H, Takeda I, Arnold JG, Mori Y, Jeong J, Kannan N, Hoffman D (2012) Impact of suspended sediment and nutrient loading from land uses against water quality in the Hii River basin, Japan. J Hydrol 450–451:25–35

    Article  Google Scholar 

  • Suess E (1973) Interaction of organic compounds with calcium carbonate-II. Organo-carbonate association in recent sediments. Geochim Cosmochim Acta 37:2435–2447

    Article  CAS  Google Scholar 

  • Thornton SF, McManus J (1994) Application of organic carbon and nitrogen stable isotope and C/N ratios as source indicators of organic matter provenance in estuarine systems: evidence from the Tay Estuary, Scotland. Estuar Coast Shelf Sci 38:219–233

    Article  CAS  Google Scholar 

  • Viaroli P, Naldi M, Christian RR, Fumagalli I (1993) The role of macroalgae and detritus in nutrient cycles in a shallow-water dystrophic lagoon. Verh Int Verein Limnol 25:1048–1051

    CAS  Google Scholar 

  • Vizzini S, Savona B, Do Chi T, Mazzola A (2005) Spatial variability of stable carbon and nitrogen isotope ratios in a Mediterranean coastal lagoon. Hydrobiol 550:73–82

    Article  CAS  Google Scholar 

  • Waser NAD, Harrison WG, Head EJH, Nielsen B, Lutz VA, Calvert SE (2000) Geographic variations in the nitrogen isotope composition of surface particulate nitrogen and new production across the North Atlantic Ocean. Deep-Sea Res I 47:1207–1226

    Article  CAS  Google Scholar 

  • Wentworth CK (1922) A scale of grade and class terms for classic sediments. J Geol 30:377–392

    Article  Google Scholar 

  • Yamamuro M (2000) Chemical tracers of sediment organic matter origins in two coastal lagoons. J Mar Sys 26:127–134

    Article  Google Scholar 

  • Zeng J, Yang L, Li J, Liang Y, Xiao L, Jiang L, Zhao D (2009) Vertical distribution of bacterial community structure in the sediments of two eutrophic lakes revealed by denaturing gradient gel electrophoresis (DGGE) and multivariate analysis techniques. World J Microbiol Biotechnol 25:225–233

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Yoshikuni Urushigawa for measurement of the total carbon and nitrogen, stable carbon and nitrogen isotope ratios and advice on interpretation of these data during his tenure as Professor in the Faculty of System Science and Technology at Akita Prefectural University. We also thank three anonymous reviewers for their constructive comments and suggestions, which helped improve this paper.

Author information

Author notes

  1. Shun Tsuboi

    Present address: National Institute for Environmental Studies, Tsukuba, 305-8506, Japan

  2. Narasimmalu Rajendran

    Present address: School of Bio-sciences and Technology, VIT University, Vellore, 632014, India

Authors and Affiliations

  1. Graduate School of Environment and Information Sciences, Yokohama National University, Yokohama, 240-8501, Japan

    Shun Tsuboi, Takashi Amemiya, Kiminori Itoh & Narasimmalu Rajendran

  2. Research Center for Coastal Lagoon Environments, Shimane University, Matsue, 690-8504, Japan

    Koji Seto & Narasimmalu Rajendran

Authors
  1. Shun Tsuboi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takashi Amemiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Koji Seto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kiminori Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Narasimmalu Rajendran
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shun Tsuboi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsuboi, S., Amemiya, T., Seto, K. et al. The ecological roles of bacterial populations in the surface sediments of coastal lagoon environments in Japan as revealed by quantification and qualification of 16S rDNA. World J Microbiol Biotechnol 29, 759–774 (2013). https://doi.org/10.1007/s11274-012-1231-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-012-1231-y

Keywords

Search

Navigation