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Bacterial Colonization on Fecal Pellets of Harpacticoid Copepods and on Their Diatom Food

  • Microbiology of Aquatic Systems
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Abstract

Fecal pellets make up a significant fraction of the global flux of organic matter in oceans, and the associated bacterial communities in particular are a potential food source for marine organisms. However, these communities remain largely unknown. In the present study, the bacterial communities on fecal pellets of the benthic copepod Paramphiascella fulvofasciata feeding on the diatoms Navicula phyllepta and Seminavis robusta were analyzed. The aim of this study was to characterize the bacterial communities associated with the diatoms and the fecal pellets by means of DGGE profiling. Furthermore, isolated bacteria were characterized by means of partial 16S rRNA gene sequencing. The composition of the bacterial microflora on fecal pellets was studied in terms of the effect of the original food source, the age of the fecal pellets and the copepod’s identity. Alphaproteobacteria, Flavobacteria, and Bacilli were found on the fecal pellets; whereas on diatoms, exclusively Gammaproteobacteria were identified. Especially after eating N. phyllepta, there was an important increase in bacterial diversity, although the diatom N. phyllepta harbored a less diverse bacterial community than S. robusta. Our data suggest that the additional bacteria originate from the copepod’s digestive tract and largely depends on the initial food source.

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References

  1. Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280:694

    Article  CAS  Google Scholar 

  2. Møller EF, Nielsen TG (2001) Production of bacterial substrate by marine copepods: effects of phytoplankton biomass and cell size. J Plankton Res 23:527–536

    Article  Google Scholar 

  3. Møller EF, Riemann L, Søndergaard M (2007) Bacteria associated with copepods: abundance, activity and community composition. Aquat Microb Ecol 47:99–106

    Article  Google Scholar 

  4. Tang KW (2005) Copepods as microbial hotspots in the ocean: effects of host feeding activities on attached bacteria. Aquat Microb Ecol 38:31–40

    Article  Google Scholar 

  5. Buffan-Dubau E, Carman KR (2000) Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnol Oceanogr 45:381–395

    Article  CAS  Google Scholar 

  6. Jacobsen TR, Azam F (1984) Role of bacteria in copepod fecal pellet decomposition: colonization, growth rates and mineralization. Bull Mar Sci 35:492–502

    Google Scholar 

  7. Andreassen I, Noethig EM, Wassmann P (1996) Vertical particle flux on the shelf off northern Spitsbergen, Norway. Mar Ecol Prog Ser 137:215–228

    Article  Google Scholar 

  8. Ferrante JG, Parker JI (1977) Transport of diatom frustules by copepod fecal pellets to the sediments of Lake Michigan. Limnol Oceanogr 22:92–98

    Article  Google Scholar 

  9. Turner JT (2002) Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms. Aquat Microb Ecol 27:57–102

    Article  Google Scholar 

  10. González HE, Smetacek V (1994) The possible role of the cyclopoid copepod Oithona in retarding vertical flux of zooplankton faecal material. Mar Ecol Prog Ser 113:233–246

    Article  Google Scholar 

  11. Guo B, Gu J, Ye YG, Tan YQ, Kida K, Wu XL (2007) Marinobacter segnicrescens sp nov., a moderate halophile isolated from benthic sediment of the South China Sea. Int J Syst Evol Microbiol 57:1970–1974

    Article  CAS  PubMed  Google Scholar 

  12. Rademaker JL, de Bruijn FJ (1997) Characterization and classification of microbes by rep-PCR genomic fingerprinting and computer assisted pattern analysis. In: Caetano-Anollés G, Gresshoff PM (eds) DNA markers: protocols, applications and overviews. John Wiley, New York, pp 151–171

    Google Scholar 

  13. De Troch M, Cnudde C, Vyverman W, Vanreusel A (2009) Increased production of faecal pellets by the benthic harpacticoid Paramphiascella fulvofasciata: importance of the food source. Mar Biol 156:469–477

    Article  Google Scholar 

  14. De Vuyst L, Camu N, De Winter T, Vandemeulebroecke K, Van de Perre V, Vancanneyt M, De Vos P, Cleenwerck I (2008) Validation of the (GTG)5-rep-PCR fingerprinting technique for rapid classification and identification of acetic acid bacteria, with a focus on isolates from Ghanaian-fermented cocoa beans. Int J Food Microbiol 125:79–90

    Article  PubMed  Google Scholar 

  15. De Troch M, Steinarsdóttir MB, Chepurnov V, Ólafsson E (2005) Grazing on diatoms by harpacticoid copepods: species-specific density-dependent uptake and microbial gardening. Aquat Microb Ecol 39:135–144

    Article  Google Scholar 

  16. Chepurnov VA, Mann DG, Vyverman W, Sabbe K, Danielidis DB (2002) Sexual reproduction, mating system, and protoplast dynamics of Seminavis (Bacillariophyta). J Phycol 38:1004–1019

    Article  Google Scholar 

  17. Guillard RL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chandley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26–60

    Google Scholar 

  18. Baele M, Baele P, Vaneechoutte M, Storms V, Butaye P, Devriese L, Verschraegen G, Gillis M, Haesebrouck F (2000) Application of tRNA intergenic spacer PCR for identification of Enterococcus species. J Clin Microbiol 38:4201–4207

    CAS  PubMed  Google Scholar 

  19. Van Hoorde K, Verstraete T, Vandamme P, Huys G (2008) Diversity of lactic acid bacteria in two Flemish artisan raw milk Gouda-type cheeses. Food Microbiol 25:929–935

    Article  PubMed  Google Scholar 

  20. Vanhoutte T, Huys G, De Brandt E, Swings J (2004) Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16 S rRNA gene primers. FEMS Microbiol Ecol 48:437446

    Google Scholar 

  21. De Mesel I, Derycke S, Moens T, Van der Gucht K, Vincx M, Swings J (2004) Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ Microbiol 6:733–744

    Article  PubMed  Google Scholar 

  22. Van der Gucht K, Sabbe K, De Meester L, Vloemans N, Zwart G, Gillis M, Vyverman W (2001) Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. Environ Microbiol 3:680–690

    Article  Google Scholar 

  23. Gevers D, Huys G, Swings J (2001) Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol Lett 205:31–36

    Article  CAS  PubMed  Google Scholar 

  24. Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Meth Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  25. Riemann F, Helmke E (2002) Symbiotic relations of sediment agglutinating nematodes and bacteria in detrital habitats: the enzyme-sharing concept. PSZN I: Mar Ecol 23:93–113

    Article  CAS  Google Scholar 

  26. Coenye T, Falsen E, Vancanneyt M, Hoste B, Govan JRW, Kersters K, Vandamme P (1999) Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia golardii sp. nov. Int J Syst Bacteriol 49:405–413

    Article  PubMed  Google Scholar 

  27. Heyrman J, Swings J (2001) 16S rDNA sequence analysis of bacterial isolates from biodeteriorated mural painings in the Sevilia Tomb (Necropolis of Carmona, Seville, Spain). Syst Appl Microbiol 24:417–422

    Article  CAS  PubMed  Google Scholar 

  28. Clarke KR, Gorley RN (2001) PRIMER v5: user manual/tutorial. PRIMER-E, Plymouth UK, 91 pp

    Google Scholar 

  29. Bathelt RW, Schelske CL (1983) Degradation of the peritrophic membrane of freshwater zooplankton fecal pellets. Trans Amer Microsc Soc 102:288–299

    Article  Google Scholar 

  30. Grossart H-P, Levold F, Allgaler M, Simon M, Brinkhoff T (2005) Marine diatoms species harbour distinct bacterial communities. Environ Microb 7:860–873

    Article  CAS  Google Scholar 

  31. Tang K, Dziallas C, Hutalle-Schmelzer K, Grossart H-P (2009) Effects of food on bacterial community composition associated with the copepod Acartia tonsa Dana. Biol Lett 5:549–553

    Article  PubMed  Google Scholar 

  32. Ferrante JG, Ptak DJ (1978) Heterotrophic bacteria associated with the degradation of zooplankton fecal pellets in Lake Michigan. J Great Lakes Res 4:221–225

    Article  Google Scholar 

  33. Matz C, Jürgens K (2003) Interaction of nutrient limitation and protozoans grazing determines the phenotypic structure of a bacterial community. Microb Ecol 45:384–398

    Article  CAS  PubMed  Google Scholar 

  34. Carman KR (1994) Stimulation of marine free-living and epibiotic bacterial activity by copepod excretions. FEMS Microbiol Ecol 14:255–261

    Article  Google Scholar 

  35. Gerlach SA (1978) Food-chain relationships in subtidal silty sand marine sediments and the role of meiofauna in stimulating bacterial productivity. Oecologia 33:55–69

    Article  Google Scholar 

  36. Moens T, dos Santos GAP, Thompson F, Swings J, Fonsêca-Genevois V, De Mesel I (2005) Do nematode mucus secretions affect bacterial growth? Aquat Microb Ecol 40:77–83

    Article  Google Scholar 

  37. Riemann F, Schrage M (1978) The mucus-trap hypothesis on feeding of aquatic nematodes and implications for biodegradation and sediment texture. Oecologia 34:75–88

    Article  Google Scholar 

  38. Grossmann S, Reichardt W (1991) Impact of Arenicola marina on bacteria in intertidal sediments. Mar Ecol Prog Ser 77:85–93

    Article  Google Scholar 

  39. Holmes MJ, Teo SLM, Lee FC, Khoo HW (1999) Persistent low concentrations of diarrhetic shellfish toxins in the green mussels Perna viridis from the Johor Strait, Singapore: first record of diarrhetic shellfish toxins from South-East Asia. Mar Ecol Prog Ser 181:257–268

    Article  CAS  Google Scholar 

  40. Gifford DJ, Dagg MJ (1991) The microzooplankton-mesozooplankton link: consumption of planktonic Protozoa by the calanoid copepods Acartia tonsa Dana and Neocalanus plumchrus Marukawa. Mar microb Food Webs 5:161–177

    Google Scholar 

  41. Dempsey AC, Kitting CL, Rosson RA (1989) Bacterial variability among individual penaeid shrimp digestive tracts. Crustaceana 56:267–278

    Article  Google Scholar 

  42. Harris JM (1993) The presence, nature an role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol 25:195–231

    Article  Google Scholar 

  43. Huo YY, Wang CS, Yang JY, Wu M, Xu XW (2008) Marinobacter mobilis sp. nov. and Marinobacter zhejiangensis sp. nov., halophilic bacteria isolated from the East China Sea. Int J Syst Evol Microbiol 58:2885–2889

    Article  CAS  PubMed  Google Scholar 

  44. Roh SW, Quan ZX, Nam YD, Chang HW, Kim KH, Rhee SK, Oh HM, Jeon CO, Yoon JH, Bae JW (2008) Marinobacter goseongensis sp nov., from seawater. Int J Syst Evol Microbiol 58:2866–2870

    Article  CAS  PubMed  Google Scholar 

  45. Gowing MM, Silver MV (1983) Origins and microenvironment of bacteria mediating fecal pellet decomposition in the sea. Mar Biol 73:15–23

    Article  Google Scholar 

  46. Honjo S, Roman MR (1978) Marine copepod fecal pellets: production, preservation, and sedimentation. J Mar Res 36:45–57

    Google Scholar 

  47. Pomery LR, Hanson RB, McGillevary PA, Sherr BP, Kirchman D, Deibel D (1984) Microbiology and biochemistry of fecal products of pelagic tunicates: rates and fates. Bull Mar Sci 35:426–439

    Google Scholar 

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Acknowledgements

The first author is a postdoctoral fellow of the Research Foundation-Flanders (FWO-Flanders, Belgium). The second author acknowledges a PhD grant of IWT (Institute for the Promotion of Innovation by Science and Technology in Flanders). This study was conducted within the frame of research projects G.0313.04, G.0058.07, and G.0192.09 of the Research Foundation- Flanders (FWO-Flanders, Belgium). Additional support was provided by the Ghent University (BOF-GOA 01GZ0705 and BOF project 01J14809).

Special thanks to Dr. Ilse De Mesel and Mrs. Margo Cnockaert for their valuable help with the molecular analyses.

Three anonymous referees provided very valuable comments that were helped to improve a previous version of this paper.

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Authors and Affiliations

  1. Biology Department, Marine Biology, Ghent University, Campus Sterre, Krijgslaan 281–S8, 9000, Ghent, Belgium

    Marleen De Troch, Clio Cnudde, Tom Moens & Ann Vanreusel

  2. Department of Biochemistry and Microbiology, Laboratory for Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Anne Willems

Authors
  1. Marleen De Troch
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  2. Clio Cnudde
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  3. Anne Willems
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  4. Tom Moens
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  5. Ann Vanreusel
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Corresponding author

Correspondence to Marleen De Troch.

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ESM 1

Summarizing dendrogram (UPGMA) based on the Pearson correlation of the (GTG)5-PCR profiles of pure cultures isolated from diatoms and fecal pellets (fp). a-r clusters with the number of isolates in each cluster indicated between brackets) (GIF 41 kb)

High resolution image (EPS 5100 kb)

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De Troch, M., Cnudde, C., Willems, A. et al. Bacterial Colonization on Fecal Pellets of Harpacticoid Copepods and on Their Diatom Food. Microb Ecol 60, 581–591 (2010). https://doi.org/10.1007/s00248-010-9669-7

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  • DOI: https://doi.org/10.1007/s00248-010-9669-7

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