Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing

Freshwater ecosystems are critical but fragile environments directly affecting society and its welfare. However, our understanding of genuinely freshwater microbial communities, constrained by our capacity to manipulate its prokaryotic participants in axenic cultures, remains very rudimentary. Even...

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Published in:Molecular ecology Vol. 23; no. 24; pp. 6073 - 6090
Main Authors: Ghai, Rohit, Mizuno, Carolina Megumi, Picazo, Antonio, Camacho, Antonio, Rodriguez-Valera, Francisco
Format: Journal Article
Language:English
Published: England Blackwell Publishing Ltd 01-12-2014
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Summary:Freshwater ecosystems are critical but fragile environments directly affecting society and its welfare. However, our understanding of genuinely freshwater microbial communities, constrained by our capacity to manipulate its prokaryotic participants in axenic cultures, remains very rudimentary. Even the most abundant components, freshwater Actinobacteria, remain largely unknown. Here, applying deep metagenomic sequencing to the microbial community of a freshwater reservoir, we were able to circumvent this traditional bottleneck and reconstruct de novo seven distinct streamlined actinobacterial genomes. These genomes represent three new groups of photoheterotrophic, planktonic Actinobacteria. We describe for the first time genomes of two novel clades, acMicro (Micrococcineae, related to Luna2,) and acAMD (Actinomycetales, related to acTH1). Besides, an aggregate of contigs belonged to a new branch of the Acidimicrobiales. All are estimated to have small genomes (approximately 1.2 Mb), and their GC content varied from 40 to 61%. One of the Micrococcineae genomes encodes a proteorhodopsin, a rhodopsin type reported for the first time in Actinobacteria. The remarkable potential capacity of some of these genomes to transform recalcitrant plant detrital material, particularly lignin‐derived compounds, suggests close linkages between the terrestrial and aquatic realms. Moreover, abundances of Actinobacteria correlate inversely to those of Cyanobacteria that are responsible for prolonged and frequently irretrievable damage to freshwater ecosystems. This suggests that they might serve as sentinels of impending ecological catastrophes.
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Spanish Ministerio de Ciencia e Innovación - No. CSD2009-00006
ArticleID:MEC12985
ark:/67375/WNG-D50Z3DL5-Z
Spanish Ministerio de Economía y Competitividad - No. BFPU2013-48007-P; No. CGL2012-38909
istex:C685B65F2E845B464C504168F37F204E5BAA5CDC
Table S1 Main environmental variables of the Amadorio reservoir corresponding to the sampled depth (10 m) on February 1st, 2012, during the mixing period. Table S2 Key residues in diverse rhodopsin sequences. Fig. S1 Vertical profiles of the main environmental variables in the Amadorio reservoir at the date of sampling (February 1st, 2012). Fig. S2 16S rRNA read classifications of the Amadorio freshwater reservoir and several other freshwater metagenomic datasets. Fig. S3 Genome size vs. GC content. Fig. S4 Genomic GC content vs. median intergenic spacer content. Fig. S5 16S rRNA phylogeny using maximum likelihood. Fig. S6 Microscopic FISH image of samples from Amadorio reservoir. Fig. S7 Abundance and size (maximum cell dimension) structure of the bacterioplankton community in the Amadorio reservoir as determined by flow cytometry. Fig. S8 Metabolic overview of the freshwater Actinobacteria acAcidi group. Fig. S9 Metabolic overview of the freshwater Actinobacteria acAMD-5. Fig. S10 Metabolic overview of the freshwater Actinobacteria acMicro-4. Fig. S11 (a) Gene cluster encoding genes for the protocatechuate degradation pathway in acMicro-1 genome. (b) The biochemical pathway of protocatechuate degradation.Data S1 (A) Metabolic pathway comparison. (B) Transporter comparison. (C) Carbohydrate-active enzyme comparison. (D) Actinobacterial core.
European Commission FP7 - No. 311975
ObjectType-Article-1
SourceType-Scholarly Journals-1
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content type line 23
ISSN:0962-1083
1365-294X
DOI:10.1111/mec.12985