Metagenomic Analysis of Subtidal Sediments from Polar and Subpolar Coastal Environments Highlights the Relevance of Anaerobic Hydrocarbon Degradation Processes

Abstract Background: Marine sediments can contain large amounts of alkanes and methylated aromatic hydrocarbons that are introduced by natural processes or anthropogenic activities. These compounds can be biodegraded by anaerobic microorganisms via enzymatic addition of fumarate. Previous gene- and genome-based surveys have detected ubiquitous and novel fumarate-adding enzymes (FAE), but these were neither confirmed as occurring within full degradation pathways nor affiliated with known organisms. The identity and ecological roles of a significant fraction of anaerobic hydrocarbon degraders in marine sediments therefore remains unknown.Results: By combining phylogenetic reconstructions, protein homolog modelling, and functional profiling of publicly available and newly sequenced metagenomes and genomes, 61 draft bacterial and archaeal genomes encoding anaerobic hydrocarbon degradation via fumarate addition were obtained. Besides Deltaproteobacteria that are well-known to catalyze these reactions, Chloroflexi are dominant FAE-encoding bacteria in hydrocarbon-impacted sediments, potentially coupling sulfate reduction or fermentation to anaerobic hydrocarbon degradation. Among Archaea, besides Archaeoglobi previously shown to have this capability, genomes of Heimdallarchaeota, Lokiarchaeota, Thorarchaeota and Thermoplasmata also suggest fermentative hydrocarbon degradation using archaea-type FAE. The biogeography survey reveals these bacterial and archaeal hydrocarbon degraders occur in a wide range of marine sediments, including high abundances of FAE-encoding Asgard archaea associated with natural seeps and subseafloor ecosystems.Conclusions: Our results expand the knowledge of novel microbial lineages engaged in anaerobic degradation of alkanes and methylated aromatic hydrocarbons, and shed new light on the importance of marine sedimentary archaea in hydrocarbon degradation.

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CANT-HYD: A curated database of phylogeny-derived Hidden Markov Models for annotation of marker genes involved in hydrocarbon degradation

10.1101/2021.06.10.447808 ◽

2021 ◽

Author(s):

Varada Khot ◽

Jackie Zorz ◽

Daniel A Gittins ◽

Anirban Chakraborty ◽

Emma Bell ◽

...

Keyword(s):

Markov Models ◽

Hydrocarbon Degradation ◽

Marker Genes ◽

Degradation Pathways ◽

Metabolic Potential ◽

Accurate Identification ◽

Isolation And Characterization ◽

Anaerobic Hydrocarbon Degradation ◽

Aliphatic And Aromatic Hydrocarbons

Discovery of microbial hydrocarbon degradation pathways has traditionally relied on laboratory isolation and characterization of microorganisms. Although many metabolic pathways for hydrocarbon degradation have been discovered, the absence of tools dedicated to their annotation makes it difficult to identify the relevant genes and predict the hydrocarbon degradation potential of microbial genomes and metagenomes. Furthermore, sequence homology between hydrocarbon degradation genes and genes with other functions often results in misannotation. A tool that systematically identifies hydrocarbon metabolic potential is therefore needed. We present the Calgary approach to ANnoTating HYDrocarbon degradation genes (CANT-HYD), a database containing HMMs of 37 marker genes involved in anaerobic and aerobic degradation pathways of aliphatic and aromatic hydrocarbons. Using this database, we show that hydrocarbon metabolic potential is widespread in the tree of life and identify understudied or overlooked hydrocarbon degradation potential in many phyla. We also demonstrate scalability by analyzing large metagenomic datasets for the prediction of hydrocarbon utilization in diverse environments. To the best of our knowledge, CANT-HYD is the first comprehensive tool for robust and accurate identification of marker genes associated with aerobic and anaerobic hydrocarbon degradation.

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Anaerobic Hydrocarbon Degradation in Petroleum-Contaminated Harbor Sediments under Sulfate-Reducing and Artificially Imposed Iron-Reducing Conditions

Environmental Science & Technology ◽

10.1021/es9600441 ◽

1996 ◽

Vol 30 (9) ◽

pp. 2784-2789 ◽

Cited By ~ 102

Author(s):

John D. Coates ◽

Robert T. Anderson ◽

Joan C. Woodward ◽

Elizabeth J. P. Phillips ◽

Derek R. Lovley

Keyword(s):

Hydrocarbon Degradation ◽

Sulfate Reducing ◽

Anaerobic Hydrocarbon Degradation ◽

Reducing Conditions ◽

Harbor Sediments

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Increment in Anaerobic Hydrocarbon Degradation Activity of Halic Bay Sediments via Nutrient Amendment

Microbial Ecology ◽

10.1007/s00248-011-9825-8 ◽

2011 ◽

Vol 61 (4) ◽

pp. 871-884 ◽

Cited By ~ 8

Author(s):

Mustafa Kolukirik ◽

Orhan Ince ◽

Bahar K. Ince

Keyword(s):

Hydrocarbon Degradation ◽

Anaerobic Hydrocarbon Degradation ◽

Degradation Activity ◽

Nutrient Amendment

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Microbial community and potential functional gene diversity involved in anaerobic hydrocarbon degradation and methanogenesis in an oil sands tailings pond

Genome ◽

10.1139/gen-2013-0083 ◽

2013 ◽

Vol 56 (10) ◽

pp. 612-618 ◽

Cited By ~ 39

Author(s):

Dongshan An ◽

Damon Brown ◽

Indranil Chatterjee ◽

Xiaoli Dong ◽

Esther Ramos-Padron ◽

...

Keyword(s):

16S Rrna ◽

Oil Sands ◽

Gene Diversity ◽

Surface Mining ◽

Hydrocarbon Degradation ◽

Metagenomic Sequencing ◽

Tailings Pond ◽

Anaerobic Hydrocarbon Degradation ◽

Phylogenetic Affiliation ◽

Oil Sands Tailings

Oil sands tailings ponds harbor large amounts of tailings resulting from surface mining of bitumen and consist of water, sand, clays, residual bitumen, and hydrocarbon diluent. Oxygen ingress in these ponds is limited to the surface layers, causing most hydrocarbon degradation to be catalyzed by anaerobic, methanogenic microbial communities. This causes the evolution of large volumes of methane of up to 104m3/day. A pyrosequencing survey of 16S rRNA amplicons from 10 samples obtained from different depths indicated the presence of a wide variety of taxa involved in anaerobic hydrocarbon degradation and methanogenesis, including the phyla Proteobacteria, Euryarchaeota, Firmicutes, Actinobacteria, Chloroflexi, and Bacteroidetes. Metagenomic sequencing of DNA isolated from one of these samples indicated a more diverse community than indicated by the 16S rRNA amplicon survey. Both methods indicated the same major phyla to be present. The metagenomic dataset indicated the presence of genes involved in the three stages of anaerobic aromatic hydrocarbon degradation, including genes for enzymes of the peripheral (upper), the central (lower), and the methanogenesis pathways. Upper pathway genes showed broad phylogenetic affiliation (Proteobacteria, Firmicutes, and Actinobacteria), whereas lower pathway genes were mostly affiliated with the Deltaproteobacteria. Genes for both hydrogenotrophic and acetotrophic methanogenesis were also found. The wide variety of taxa involved in initial hydrocarbon degradation through upper pathways may reflect the variety of residual bitumen and diluent components present in the tailings pond.

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Marine sediments harbor diverse archaea and bacteria with the potential for anaerobic hydrocarbon degradation via fumarate addition

FEMS Microbiology Ecology ◽

10.1093/femsec/fiab045 ◽

2021 ◽

Author(s):

Chuwen Zhang ◽

Rainer U Meckenstock ◽

Shengze Weng ◽

Guangshan Wei ◽

Casey R J Hubert ◽

...

Keyword(s):

Marine Sediments ◽

Aromatic Hydrocarbons ◽

Anthropogenic Activities ◽

Hydrocarbon Degradation ◽

Anaerobic Microorganisms ◽

Anaerobic Hydrocarbon Degradation ◽

Wide Range ◽

Functional Profiling ◽

Fumarate Addition ◽

Hydrocarbon Degraders

Abstract Marine sediments can contain large amounts of alkanes and methylated aromatic hydrocarbons that are introduced by natural processes or anthropogenic activities. These compounds can be biodegraded by anaerobic microorganisms via enzymatic addition of fumarate. However, the identity and ecological roles of a significant fraction of hydrocarbon degraders containing fumarate-adding enzymes (FAE) in various marine sediments remains unknown. By combining phylogenetic reconstructions, protein homolog modelling, and functional profiling of publicly available metagenomes and genomes, 61 draft bacterial and archaeal genomes encoding anaerobic hydrocarbon degradation via fumarate addition were obtained. Besides Desulfobacterota (previously known as Deltaproteobacteria) that are well-known to catalyze these reactions, Chloroflexi are dominant FAE-encoding bacteria in hydrocarbon-impacted sediments, potentially coupling sulfate reduction or fermentation to anaerobic hydrocarbon degradation. Among Archaea, besides Archaeoglobi previously shown to have this capability, genomes of Heimdallarchaeota, Lokiarchaeota, Thorarchaeota and Thermoplasmata also suggest fermentative hydrocarbon degradation using archaea-type FAE. These bacterial and archaeal hydrocarbon degraders occur in a wide range of marine sediments, including high abundances of FAE-encoding Asgard archaea associated with natural seeps and subseafloor ecosystems. Our results expand the knowledge of diverse archaeal and bacterial lineages engaged in anaerobic degradation of alkanes and methylated aromatic hydrocarbons.

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