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Microbial Ecology

, Volume 71, Issue 1, pp 100–112 | Cite as

Diverse Bacterial Groups Contribute to the Alkane Degradation Potential of Chronically Polluted Subantarctic Coastal Sediments

  • Lilian M. Guibert
  • Claudia L. Loviso
  • Sharon Borglin
  • Janet K. Jansson
  • Hebe M. Dionisi
  • Mariana Lozada
Environmental Microbiology

Abstract

We aimed to gain insight into the alkane degradation potential of microbial communities from chronically polluted sediments of a subantarctic coastal environment using a combination of metagenomic approaches. A total of 6178 sequences annotated as alkane-1-monooxygenases (EC 1.14.15.3) were retrieved from a shotgun metagenomic dataset that included two sites analyzed in triplicate. The majority of the sequences binned with AlkB described in Bacteroidetes (32 ± 13 %) or Proteobacteria (29 ± 7 %), although a large proportion remained unclassified at the phylum level. Operational taxonomic unit (OTU)-based analyses showed small differences in AlkB distribution among samples that could be correlated with alkane concentrations, as well as with site-specific variations in pH and salinity. A number of low-abundance OTUs, mostly affiliated with Actinobacterial sequences, were found to be only present in the most contaminated samples. On the other hand, the molecular screening of a large-insert metagenomic library of intertidal sediments from one of the sampling sites identified two genomic fragments containing novel alkB gene sequences, as well as various contiguous genes related to lipid metabolism. Both genomic fragments were affiliated with the phylum Planctomycetes, and one could be further assigned to the genus Rhodopirellula due to the presence of a partial sequence of the 23S ribosomal RNA (rRNA) gene. This work highlights the diversity of bacterial groups contributing to the alkane degradation potential and reveals patterns of functional diversity in relation with environmental stressors in a chronically polluted, high-latitude coastal environment. In addition, alkane biodegradation genes are described for the first time in members of Planctomycetes.

Keywords

Alkane monooxygenase Coastal sediments Bacteroidetes Actinomycetes Planctomycetes Metagenomics 

Notes

Acknowledgments

At the time of this study, LMG and CLL were recipients of a graduate student fellowship from the Argentinean National Research Council (CONICET). ML and HMD are staff members from CONICET. This work was funded by grants from CONICET, the National Agency for the Promotion of Science and Technology (ANPCyT, Argentina) and by the Pacific Northwest National Laboratory under contract number DE-AC05-76RL01830. Shotgun sequencing and annotation were conducted through the Community Sequencing Program (CSP 328) of the US Department of Energy Joint Genome Institute (JGI), a DOE Office of Science User Facility under Contract No. DE-AC02-05CH11231. We would like to thank Ricardo Vera and Horacio Ocariz for their help in sample collection.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2015_698_MOESM1_ESM.pdf (114 kb)
Online Resource 1 Supplementary materials and methods (PDF 114 kb)
248_2015_698_MOESM2_ESM.pdf (64 kb)
Online Resource 2 Details of OTU-based analysis of 16S rRNA gene amplicon sequences (PDF 64 kb)
248_2015_698_MOESM3_ESM.pdf (78 kb)
Online Resource 3 Taxonomic assignment of the most abundant 16S rRNA gene amplicon sequences using QIIME (PDF 78 kb)
248_2015_698_MOESM4_ESM.pdf (76 kb)
Online Resource 4 Details of OTU-based analysis of putative AlkB sequences identified in the metagenomic dataset (PDF 76 kb)
248_2015_698_MOESM5_ESM.pdf (128 kb)
Online Resource 5 Relative abundance of OTUs of putative AlkB sequences (PDF 127 kb)
248_2015_698_MOESM6_ESM.pdf (88 kb)
Online Resource 6 Complete names of the reference AlkB sequences used for phylogenetic placement (PDF 88 kb)
248_2015_698_MOESM7_ESM.pdf (28 kb)
Online Resource 7 Results of the phylogenetic placement using the complete AlkB dataset. The tree was constructed by maximum likelihood in RAxML v.8.2.3 and visualized in pplacer/guppy. Reference sequences used for placement are indicated with their GenBank accession number. The full names are provided in Online Resource 6. In red, branches where sequences have been placed, with the width of these branches being proportional to the number of sequences placed in that branch. The likelihood weight ratio (a measure of the certainty of the placement of the sequences [69]) was 0.53 ± 0.27 (PDF 28 kb)
248_2015_698_MOESM8_ESM.pdf (73 kb)
Online Resource 8 Alignment of full-length AlkB sequences identified in the metagenomic dataset and in the fosmid library. The positions of the four conserved histidine-containing motifs (His 1, His 2, HYG, and His 3), and of the six transmembrane segments (I–VI) are indicated by boxes and dotted lines, respectively. CAB54050: Pseudomonas putida GPo1 alkane-1 - monooxygenase (PDF 73 kb)
248_2015_698_MOESM9_ESM.pdf (104 kb)
Online Resource 9 Details of the coding sequences predicted in fosmid clones No. 401 and 964 (PDF 103 kb)
248_2015_698_MOESM10_ESM.pdf (28 kb)
Online Resource 10 Phylogenetic analysis of the 23S rRNA gene fragment from fosmid No. 401 and related sequences from strains belonging to the Planctomycetes phylum. The tree was constructed with MEGA 5 software using the Maximum Likelihood algorithm. The GenBank accession number of the reference sequences is indicated first. The sequence fragment from this study is shown in bold type. Only bootstrap values ≥70 % (1000 repetitions) are shown. Sequences from members of Verrucomicrobia, Bacteroidetes, Chlamydia, and Lentisphaera phyla were used as outgroup. The scale bar represents 0.05 nucleotide substitutions per site (PDF 28 kb)

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Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Lilian M. Guibert
    • 1
  • Claudia L. Loviso
    • 1
  • Sharon Borglin
    • 2
  • Janet K. Jansson
    • 3
  • Hebe M. Dionisi
    • 1
  • Mariana Lozada
    • 1
  1. 1.Laboratorio de Microbiología AmbientalCentro para el Estudio de Sistemas Marinos (CESIMAR, CENPAT-CONICET)Puerto MadrynArgentina
  2. 2.Energy Geosciences DivisionLawrence Berkeley National LaboratoryBerkeleyUSA
  3. 3.Earth and Biological Sciences DirectoratePacific Northwest National LaboratoryRichlandUSA

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