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Bacterial diversity of the sediments transiting through the gut of Holothuria scabra (Holothuroidea; Echinodermata)

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Abstract

This work analyzes bacterial diversity of sediments transiting through the gut of Holothuria scabra which is an important bioturbator in tropical shallow waters. This edible holothurian species has a social and economic importance for coastal populations in many developing countries. Bacterial biodiversity was analyzed by sequencing the 16S rRNA of bacterial cultures and clones. DAPI and FISH methods were used to determine and compare the number of bacteria found in the various gut compartments. A total of 116 phylotypes belonging to the γ-Proteobacteria (60.5 %), α-Proteobacteria (24.5 %), Bacteroidetes (6 %), Actinobacteria (2.75 %), Fusobacteria (1.75 %), Firmicutes (1.75 %), Cyanobacteria (1.75 %) and δ-Proteobacteria (1 %) were identified. The number of bacteria is significantly greater (1.5×) in the foregut than in the ambient sediments. The number of bacteria significantly decreases in the midgut and remains stable until defecation. Some γ-Proteobacteria, especially Vibrio, are less affected by digestion than other bacterial taxa. The season has an impact on the bacterial diversity found in the sediments transiting through the gut: in the dry season, γ-Proteobacteria are the most abundant taxon, while α-Proteobacteria dominate in the rainy season. Vibrio is the most frequent genus with some well-known opportunistic pathogens like V. harveyi, V. alginolyticus and V. proteolyticus. Findings show that sediment-associated microbial communities are significantly modified by H. scabra during their transit through the gut which supports the view that holothurians play a substantial role in the structuring of bacterial communities at the sediment–seawater interface.

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Acknowledgments

We wish to thank the FNRS (Fonds National pour la Recherche Scientifique), CUD (Commission Universitaire pour le Développement) and AMPA (Agence Malgache de la Pêche et de l’Aquaculture) for financing assignments in Madagascar. T.P. benefited from a doctoral grant of the FRIA (Fonds pour la formation à la Recherche dans l’Industrie et l’Agriculture). This work is a contribution of the CIBIM (Centre Interuniversitaire de Biologie Marine) and of the PRU (Polyaquaculture Research Unit). We thank very much Jean-François Hamel and Annie Mercier for checking the English and two anonymous reviewers for their useful comments.

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Authors and Affiliations

  1. Biology of Marine Organisms and Biomimetism Lab, University of Mons, 7000, Mons, Belgium

    Thomas Plotieau & Igor Eeckhaut

  2. Haute Ecole Provinciale de Hainaut, Condorcet, 7000, Mons, Belgium

    Thomas Plotieau

  3. Polyaquaculture Research Unit, IHSM, University of Toliara, 601, Toliara, Madagascar

    Thierry Lavitra & Igor Eeckhaut

  4. Proteomics and Microbiology Lab, University of Mons, 7000, Mons, Belgium

    David C. Gillan

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  1. Thomas Plotieau
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Correspondence to Igor Eeckhaut.

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227_2013_2297_MOESM1_ESM.eps

Fig. 1S. Distance tree showing the relationships among the 16S rRNA clones and isolates of the γ-Proteobacteria obtained in this study. The bacteria indicated by names in the tree are those whose similarity is higher than 99 % during a blast search. Green nonsulfur bacterium served as the outgroup. A matrix of 121 OTUs was used. GenBank accession numbers are listed for the close relatives of the clones and isolates. Bootstrap values are shown above branches (1000 replicates). The origin of bacteria are indicated in brackets: (SW) = seawater, (S) = substrate, (F) = foregut, (M) = midgut, (H) = hindgut and (Fa) = faeces. (EPS 36204 kb)

227_2013_2297_MOESM2_ESM.eps

Fig. 2S. Distance tree showing the relationships among the 16S rRNA clones and isolates of Cyanobacteria, Actinobacteria, Firmicutes, α-Proteobacteria, δ-Proteobacteria, Fusobacteria and Bacteroidetes obtained in this study. The bacteria indicated by names in the tree are those whose similarity is higher than 99 % during a blast search. Green nonsulfur bacterium served as the outgroup. A matrix of 76 OTUs was used. GenBank accession numbers are listed for the close relatives of the clones and isolates. Bootstrap values are shown above branches (1000 replicates). The origin of bacteria are indicated in brackets: (SW) = seawater, (S) = substrate, (F) = foregut, (M) = midgut, (H) = hindgut and (Fa) = faeces. (EPS 9263 kb)

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Plotieau, T., Lavitra, T., Gillan, D.C. et al. Bacterial diversity of the sediments transiting through the gut of Holothuria scabra (Holothuroidea; Echinodermata). Mar Biol 160, 3087–3101 (2013). https://doi.org/10.1007/s00227-013-2297-2

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