Microbial Ecology

, Volume 70, Issue 4, pp 889–903 | Cite as

Composition and Predictive Functional Analysis of Bacterial Communities in Seawater, Sediment and Sponges in the Spermonde Archipelago, Indonesia

  • Daniel F. R. Cleary
  • Nicole J. de Voogd
  • Ana R. M. Polónia
  • Rossana Freitas
  • Newton C. M. Gomes
Microbiology of Aquatic Systems


In this study, we used a 16S rRNA gene barcoded pyrosequencing approach to sample bacterial communities from six biotopes, namely, seawater, sediment and four sponge species (Stylissa carteri, Stylissa massa, Xestospongia testudinaria and Hyrtios erectus) inhabiting coral reefs of the Spermonde Archipelago, South Sulawesi, Indonesia. Samples were collected along a pronounced onshore to offshore environmental gradient. Our goals were to (1) compare higher taxon abundance among biotopes, (2) test to what extent variation in bacterial composition can be explained by the biotope versus environment, (3) identify dominant (>300 sequences) bacterial operational taxonomic units (OTUs) and their closest known relatives and (4) assign putative functions to the sponge bacterial communities using a recently developed predictive metagenomic approach. We observed marked differences in bacterial composition and the relative abundance of the most abundant phyla, classes and orders among sponge species, seawater and sediment. Although all biotopes housed compositionally distinct bacterial communities, there were three prominent clusters. These included (1) both Stylissa species and seawater, (2) X. testudinaria and H. erectus and (3) sediment. Bacterial communities sampled from the same biotope, but different environments (based on proximity to the coast) were much more similar than bacterial communities from different biotopes in the same environment. The biotope thus appears to be a much more important structuring force than the surrounding environment. There were concomitant differences in the predicted counts of KEGG orthologs (KOs) suggesting that bacterial communities housed in different sponge species, sediment and seawater perform distinct functions. In particular, the bacterial communities of both Stylissa species were predicted to be enriched for KOs related to chemotaxis, nitrification and denitrification whereas bacterial communities in X. testudinaria and H. erectus were predicted to be enriched for KOs related to the toxin–antitoxin (TA) system, nutrient starvation and heavy metal export.


16S rRNA gene KEGG orthologs Makassar Ordination Pyrosequencing 



This research was supported by the Portuguese Foundation for Science and Technology (FCT) under grant PTDC/AAC-AMB/115304/2009 (LESS CORAL) and a PhD Fellowship SFRH/BD/33391/2008. Samples were collected under a research permit issued by the Indonesian State Ministry for Research and Technology (Kementerian Riset Dan Teknologi Republik Indonesia (RISTEK)). We thank the Indonesian Institute of Sciences (PPO-LIPI) for their support and especially Yos Tuti.

Supplementary material

248_2015_632_MOESM1_ESM.pdf (113 kb)
Online Resource 1 (PDF 113 kb)
248_2015_632_MOESM2_ESM.pdf (7 kb)
Online Resource 2 Stacked barplot showing the relative abundances of the nine most abundant phyla sampled from the six biotopes, a) S. carteri, b) S. massa, c) X. testudinaria, d) H. erectus, e) Sediment and f) Seawater. The site codes (x axis) are Lae: Lae Lae, Sam: Samalona, Kud: Kudingkareng Keke, Bak: Bone Baku and Lan: Langkai (PDF 7.10 kb)
248_2015_632_MOESM3_ESM.xls (18 kb)
Online Resource 3 List of most abundant OTUs (>300 sequences) including OTU-numbers; total sequences (Sum) and the subtotals for samples from seawater (Wt); sediment (Sd); S. massa (Sm); S. carteri (Sc); X. testudinaria (Xt); H. erectus (He); taxonomic affiliation of OTU, GenBank GenInfo sequence identifiers (GI) of closely related organisms identified using BLAST; sequence identity (Sq ident) of these organisms with our representative OTU sequences; isolation source (Source) of closely related organisms identified using BLAST; location where the isolation source was sampled (Location). (XLS 18 kb)
248_2015_632_MOESM4_ESM.pdf (19 kb)
Online Resource 4 Maximum Likelihood phylogenetic tree (16S rRNA gene sequences) of the most dominant OTUs(Table 1) assigned to the phylum Proteobacteria and their cultured closest relatives (gi = GeneBank sequence identification number). Symbols represent samples from seawater (Wt), sediment (Sd), S. massa (Sm), S. carteri (Sc), X. testudinaria (Xt) and H. erectus (He). Bootstrap values generated from 500 replicates. Bootstrap values lower than 50 % were omitted. For the analysis, selected 16S rRNA gene sequences of the most dominant OTUs (≥300 sequences) and their cultured closest relatives in GenBank [] were aligned using ClustalW and a phylogenetic analysis conducted using MEGA 6 software ( (Tamura et al., 2011). Phylogenetic trees were constructed according to the maximum-likelihood statistical method using the general time reversible (GTR) model with a discrete Gamma distribution (5 categories (+G, parameter = 0.4305). In the results, we present a bootstrap consensus tree based on 500 replicates. The bootstrap value is shown next to each branch when this exceeds 49 %. This value represents the percentage of replicate trees in which the associated taxa clustered together. For tree inference we used the nearest neighbor interchange (NNI) heuristic method and automatic initial tree selection. (PDF 18 kb)
248_2015_632_MOESM5_ESM.pdf (10 kb)
Online Resource 5 Maximum Likelihood phylogenetic tree (16S rRNA gene sequences) of the most dominant OTUs(Table 1) assigned to the non-proteobacterial phyla and their cultured closest relatives (gi = GeneBank sequence identification number). Symbols represent samples from seawater (Wt), sediment (Sd), S. massa (Sm), S. carteri (Sc), X. testudinaria (Xt) and H. erectus (He). Bootstrap values generated from 500 replicates. Bootstrap values lower than 50 % were omitted. (PDF 10 kb)
248_2015_632_MOESM6_ESM.pdf (8 kb)
Online Resource 6 Stacked bar plots showing the estimated gene count (Y axis) of a set of KOs and the contribution of selected orders to the gene count; unclassified OTUs at the order level and OTUs belonging to all other orders are pooled and indicated by ‘Other’. a) K00087 (xanthine dehydrogenase molybdenum-binding subunit), b) K03409 (chemotaxis protein CheX), c) K04561 (nitric oxide reductase) and d) K10535 (hydroxylamine oxidase) for all samples (X axis). (PDF 7 kb)
248_2015_632_MOESM7_ESM.pdf (10 kb)
Online Resource 7 Stacked bar plots showing the estimated gene count (Y axis) of a set of KOs and the contribution of selected orders to the gene count; unclassified OTUs at the order level and OTUs belonging to all other orders are pooled and indicated by ‘Other’. a) K05522 (endonuclease VIII), b) K07239 (heavy metal exporter), c) K07334 (proteic killer suppression protein) and d) K07665 (copper resistance phosphate regulon response regulator CusR) for all samples (X axis). (PDF 9 kb)


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Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Daniel F. R. Cleary
    • 1
  • Nicole J. de Voogd
    • 2
  • Ana R. M. Polónia
    • 1
  • Rossana Freitas
    • 1
  • Newton C. M. Gomes
    • 1
  1. 1.Departamento de Biologia, Centro de Estudos do Ambiente e do Mar (CESAM)Universidade de AveiroAveiroPortugal
  2. 2.Naturalis Biodiversity CenterLeidenThe Netherlands

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