"Candidatus Macondimonas diazotrophica", a novel gammaproteobacterial genus dominating crude-oil-contaminated coastal sediments

Abstract

Modeling crude-oil biodegradation in sediments remains a challenge due in part to the lack of appropriate model organisms. Here we report the metagenome-guided isolation of a novel organism that represents a phylogenetically narrow (>97% 16S rRNA gene identity) group of previously uncharacterized, crude-oil degraders. Analysis of available sequence data showed that these organisms are highly abundant in oiled sediments of coastal marine ecosystems across the world, often comprising ~30% of the total community, and virtually absent in pristine sediments or seawater. The isolate genome encodes functional nitrogen fixation and hydrocarbon degradation genes together with putative genes for biosurfactant production that apparently facilitate growth in the typically nitrogen-limited, oiled environment. Comparisons to available genomes revealed that this isolate represents a novel genus within the Gammaproteobacteria, for which we propose the provisional name "Candidatus Macondimonas diazotrophica" gen. nov., sp. nov. "Ca. M. diazotrophica" appears to play a key ecological role in the response to oil spills around the globe and could be a promising model organism for studying ecophysiological responses to oil spills.

Fig. 1

Relative abundance of MAG-01 in oiled and clean beach sands from Pensacola beach, Florida (USA). a Abundance profiles of 16S rRNA gene-based OTUs detected in pre-oil, oiled and clean samples a year after the DWH oil spill. The MAG-01 16S-OTU is shown in black, at the bottom of the columns (denoted by an asterisk). Only the top 250 most abundant OTUs are shown. b Average coverage, representing relative abundance, of MAG-01 sequence (x-axis) by the reads of the metagenomic datasets described in [23] (y-axis). c (Bottom) Read recruitment plot showing where metagenomic reads of a contaminated sample (OS_G), which had the highest abundance of MAG-01, mapped (x-axis) and their identity (y-axis). (Top) The dark blue histogram represents coverage, i.e., how many times each nucleotide base is covered by reads on average, by reads matching the reference MAG-01 sequence, at ≥80 bp in length and ≥95% nucleotide identity, in 1000 bp-long windows; light blue represents reads matching at <95% identity. The evenness of the coverage of the genome on the metagenomic datasets shows a sequence-discrete population. Note that the coverage values shown in panel (b) are derived from the average coverage obtained in the recruitment plots (dark blue histogram, Panel (c)) after normalizing for the size of the metagenomic dataset, and that the MAG-01 is not detectable in pre-spill samples and has low abundance in metagenomes of recovered microbial communities

Fig. 2

Phylogeny and distribution of KTK-01-like 16S rRNA gene sequences in oil-contaminated sites across the globe. Pie charts represent the fraction of total sequences showing >97% nucleotide identity to the 16S rRNA gene sequence of KTK-01. For instance, 30% of the OTUs recovered from the beach sands impacted by Macondo oil matched the 16S rRNA gene sequence at this level. Accession numbers of the datasets used are provided in Supplementary Table S1. Inset: 16S rRNA gene phylogeny of KTK-01 and selected close relatives. Maximum likelihood, as implemented in RaxML and using all homologous positions of the bacterial alignment in the LTP_123 dataset, was used to obtain the phylogenetic tree shown. Bootstrap values are indicated next to the branches. Complete 16S rRNA phylogeny is shown in Suppl. Fig. S4