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Marine Biology

, Volume 148, Issue 3, pp 541–550 | Cite as

Microbial reaction rates and bacterial communities in sediment surrounding burrows of two nereidid polychaetes (Nereisdiversicolor and N. virens)

  • Sokratis Papaspyrou
  • Trine Gregersen
  • Erik Kristensen
  • Bjarne Christensen
  • Raymond P. Cox
Research Article

Abstract

The effects of infaunal mode of life on sediment properties, microbial reaction rates, as well as abundance and composition of bacterial communities were studied in sediment surrounding burrows (mucus lining, oxidised wall, ambient anoxic and surface sediment) of two closely related, but behaviourally different, nereidid polychaete worms: the facultative suspension-feeder Nereis (Hediste) diversicolor and the obligate deposit-feeder Nereis (Neanthes) virens. Burrow sediment of the two species was collected from two adjacent (50 m distance) shallow sandy locations (Kertinge Nor, Denmark). The burrow lining and wall of both polychaete species were enriched in organic matter originating from mucous secretions by the inhabitants and phytoplankton trapped through irrigation. This was more evident for N. diversicolor that shows a significantly higher irrigation rate than N. virens. Both the organic matter mineralisation rates (based on anaerobic incubations) and bacterial abundance were higher along the burrow linings and walls. However, accumulation of porewater TCO2 and dissolved organic carbon in sediments adjacent to burrows increased most rapidly in the presence of N. diversicolor, suggesting higher heterotrophic activity associated with this species. Surprisingly, bacterial abundance was lower around burrows of N. diversicolor than those from N. virens indicating that burrow environments from the first species harbour a more active bacterial community. Molecular fingerprints of the 16S rRNA gene from bacterial communities showed that the composition of the burrow linings and walls resembled the ambient anoxic sediment rather than the oxic sediment surface. On the other hand, the bacterial fingerprints of the sediment surrounding the burrows of the two polychaete species were markedly different suggesting either a site-specific difference in sediment parameters or a significant species-specific impact of the burrow inhabitants.

Keywords

Bacterial Community Polychaete Meiofauna Bacterial Abundance Polychaete Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by a grant to EK (Grant#21020463) from the Danish Science Research Council and a traveling grant to SP from The Eleni Nakou Foundation.

References

  1. Aller RC (1988) Benthic fauna and biogeochemical processes in marine sediments: the role of burrow structures. In: Blackburn TH, Sorensen J (eds) Nitrogen cycling in coastal marine environments.Wiley, Chichester, pp301–338Google Scholar
  2. Aller JY, Aller RC (1986) Evidence for localized enhancement of biological activity associated with tube and burrow structures in deep-sea sediments at the HEBBLE site, western North Atlantic. Deep Sea Res 33:755–790CrossRefGoogle Scholar
  3. Aller RC, Aller JY (1998) The effect of biogenic irrigation intensity and solute exchange on diagenetic reaction rates in marine sediments. J Mar Res 56:905–936CrossRefGoogle Scholar
  4. Alongi DM (1985) Microbes, meiofauna, and bacterial productivity on the tubes constructed by the polychaete Capitella capitata. Mar Ecol Prog Ser 23:207–208CrossRefGoogle Scholar
  5. Andresen M, Kristensen E (2002) The importance of bacteria and microalgae in the diet of the deposit-feeding polychate Arenicola marina. Ophelia 56:179–196CrossRefGoogle Scholar
  6. Ausubel FW, Brent R, Kingston RE, Moore DD, Seidman JG, Struhl K, Smith JA (1995) Short protocols in molecular biology. John Wiley and Sons, New YorkGoogle Scholar
  7. Bird FL, Boon PI, Nichols PD (2000) Physicochemical and microbial properties of burrows of the deposit-feeding Thalassinidean ghost shrimp Biffarius arenosus (Decapoda: Callianassidae). Estuar Coast Shelf Sci 51:279–291CrossRefGoogle Scholar
  8. Bower CE, Holm-Hansen T (1980) A salicylate-hypochlorite method for determining ammonia in seawater. Can J Fish Aquat Sci 37:794–798CrossRefGoogle Scholar
  9. Christensen B, Vedel A, Kristensen E (2000) Carbon and nitrogen fluxes in sediment inhabited by suspension-feeding (Nereis diversicolor) and non-suspension feeding (N.virens) polychaetes. Mar Ecol Prog Ser 192:203–217CrossRefGoogle Scholar
  10. Defretin R (1971) The tubes of polychaete Annelids. In: Florkin M, Stotz EH (eds) Comprehensive biochemistry, vol. 26.2, Elsevier, Amsterdam, pp713–747Google Scholar
  11. Dobbs FC, Guckert JB (1988) Callianassa trilobata (Crustacea: Thalassinidea) influences abundance of meiofauna and biomass, composition, and physiologic state of microbial communities within its burrow. Mar Ecol Prog Ser 45:69–79CrossRefGoogle Scholar
  12. Fenchel T (1996) Worm burrows and oxic microniches in marine sediments. I. Spatial and temporal scales. Mar Biol 127:289–295CrossRefGoogle Scholar
  13. Hall PJO, Aller RC (1992) Rapid, small-volume, flow injection analysis for TCO2 and NH4+ in marine and freshwaters. Limnol Oceanogr 37:1113–1119CrossRefGoogle Scholar
  14. Hansen K, Kristensen E (1998) The impact of the polychaete Nereis diversicolor and enrichment with macroalgal (Chaetomorpha linum) detritus on benthic metabolism and nutrient dynamics in organic-poor and organic-rich sediment. J Exp Mar Biol Ecol 231:201–223CrossRefGoogle Scholar
  15. de Jonge VE (1980) Fluctuations in the organic carbon to chlorophyll a ratios for estuarine benthic diatom populations. Mar Ecol Prog Ser 2:345–353CrossRefGoogle Scholar
  16. Kristensen E (1988) Factors influencing the distribution of nereid polychaetes in Danish coastal waters. Ophelia Suppl 29:127–140CrossRefGoogle Scholar
  17. Kristensen E (2000) Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426:1–24CrossRefGoogle Scholar
  18. Kristensen E, Holmer M (2001) Decomposition of plant materials in marine sediment exposed to different electron acceptors (O2, NO3, and SO42−), with emphasis on substrate origin, degradation kinetics, and the role of bioturbation. Geochim Cosmochim Acta 65:419–433CrossRefGoogle Scholar
  19. Kristensen E, Kostka JE (2005) Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. In: Kristensen E et al (eds) Interactions between macro- and microorganisms in marine sediments. American Geophysical Union, Washington (in press)Google Scholar
  20. Kristensen E, Jensen MH, Andersen TK (1985) The impact of polychaete (Nereis virens Sars) burrows on nitrification and nitrate reduction in estuarine sediments. J Exp Mar Biol Ecol 85:75–91CrossRefGoogle Scholar
  21. Lucas FS, Bertru G, Höfle MG (2003) Characterization of free-living and attached bacteria in sediments colonized by Hediste diversicolor. Aquat Microb Ecol 32:165–174CrossRefGoogle Scholar
  22. Mackin JE, Aller RC (1984) Ammonium adsorption in marine sediments. Limnol Oceanogr 29:250–257CrossRefGoogle Scholar
  23. Marinelli RL, Lovell CR, Wakeham SG, Ringelberg DB, White DC (2002) Experimental investigation of the control of bacterial community composition in macrofaunal burrows. Mar Ecol Prog Ser 235:1–13CrossRefGoogle Scholar
  24. Mayer MS, Schaffner L, Kemp WM (1995) Nitrification potentials of benthic macrofaunal tubes and burrow walls: effects of sediment NH4+ and animal irrigation behavior. Mar Ecol Prog Ser 121:157–169CrossRefGoogle Scholar
  25. Miller DN (2001) Evaluation of gel filtration resins for the removal of PCR-inhibitory substances from soils and sediments. J Microbiol Meth 44:49–58CrossRefGoogle Scholar
  26. Miron G, Kristensen E (1993) Factors influencing the distribution of nereid polychaetes: the sulfide aspect. Mar Ecol Prog Ser 93:143–153CrossRefGoogle Scholar
  27. Muyzer G, de Waal E, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rDNA. Appl Environ Microbiol 59:695–700PubMedPubMedCentralGoogle Scholar
  28. Olivier M, Desrosiers G, Caron A, Retière C, Caillou A (1995) Responses comportementales des polychètes Nereis diversicolor (O.F. Müller) et Nereis virens (Sars) aux stimuli d’ordre alimentaire: utilisation de la matière organique particulaire (algues et halophytes). Can J Zool 73:2307–2317CrossRefGoogle Scholar
  29. Overmann J, Tuschak C (1997) Phylogeny and molecular fingerprinting of green sulfur bacteria. Arch Microbiol 167:302–309CrossRefGoogle Scholar
  30. Papaspyrou S, Gregersen T, Cox RP, Thessalou-Legaki M, Kristensen E (2005) Sediment properties and bacterial community in the burrows of the mud shrimp Pestarella tyrrhena (Decapoda: Thalassinidea). Aquat Microb Ecol 38:181–190CrossRefGoogle Scholar
  31. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, OxfordGoogle Scholar
  32. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  33. Reichardt W (1989) Microbiological aspects of bioturbation. In: Ros JD (ed) Topics in marine biology. Scient Mar 53:301–306Google Scholar
  34. Reise K (1981) High abundance of small zoobenthos around biogenic structures in tidal sediments of the Wadden Sea. Helgol Meeresunters 34:413–425CrossRefGoogle Scholar
  35. Riisgård HU, Christensen PB, Olesen NJ, Petersen JK, Moller MM, Andersen P (1995) Biological structure in a shallow cove (Kertinge-Nor, Denmark)—Control by benthic nutrient fluxes and suspension-feeding ascidians and jellyfish. Ophelia 41:329–344CrossRefGoogle Scholar
  36. Schäfer H, Muyzer G (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. Meth Microbiol 30:425–468CrossRefGoogle Scholar
  37. Sternberg SR (1983) Biomedical image processing. Computer 16:22–34CrossRefGoogle Scholar
  38. Steward CC, Nold SC, Ringelberg DB, White DC, Lovell CR (1996) Microbial biomass and community structures in the burrows of bromophenol producing and non-producing marine worms and surrounding sediments. Mar Ecol Prog Ser 133:149–165CrossRefGoogle Scholar
  39. Vedel A, Riisgård HU (1993) Filter-feeding in the polychaete Nereis diversicolor: growth and bioenergetics. Mar Ecol Prog Ser 100:145–152CrossRefGoogle Scholar
  40. Zola H (1967) Sugar phosphate polymers in polychaete tubes and in mineralized animal tissues. Comp Biochem Physiol 21:179–183CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Sokratis Papaspyrou
    • 1
  • Trine Gregersen
    • 2
  • Erik Kristensen
    • 3
  • Bjarne Christensen
    • 3
  • Raymond P. Cox
    • 2
  1. 1.Department of Zoology-Marine Biology, Faculty of BiologyUniversity of AthensAthensGreece
  2. 2.Department of Biochemistry and Molecular BiologyUniversity of Southern DenmarkOdense MDenmark
  3. 3.Institute of BiologyUniversity of Southern DenmarkOdense MDenmark

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