Fermentative Spirochaetes mediate necromass recycling in anoxic hydrocarbon-contaminated habitats

Dong, Xiyang; Greening, Chris; Brüls, Thomas; Conrad, Ralf; Guo, Kun; Blaskowski, Svenja; Kaschani, Farnusch; Kaiser, Markus; Laban, Nidal Abu; Meckenstock, Rainer U.

doi:10.1038/s41396-018-0148-3

Cited by 70 publications

(58 citation statements)

References 57 publications

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“…Other members in culture TRIP1 include Spirochaetes, members of which (e.g., Spirochaetaceae) are often found in anaerobic cultures capable of degrading aromatic compounds and have been identified in sediment, ground-and freshwater samples. Their role of these Spirochaetes appears related to necromass fermentation, leading to a microbial loop recycling nutrients (Koelschbach et al, 2017;Dong et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Anaerobic degradation of phenanthrene by a sulfate‐reducing enrichment culture

Himmelberg

Brüls

Farmani

et al. 2018

Environmental Microbiology

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Anaerobic degradation processes are very important to attenuate polycyclic aromatic hydrocarbons (PAHs) in saturated, anoxic sediments. However, PAHs are poorly degradable, leading to very slow microbial growth and thus resulting in only a few cultures that have been enriched and studied so far. Here, we report on a new phenanthrene-degrading, sulfate-reducing enrichment culture, TRIP1. Genome-resolved metagenomics and strain specific cell counting with FISH and flow cytometry indicated that the culture is dominated by a microorganism belonging to the Desulfobacteraceae family (60% of the community) and sharing 93% 16S rRNA sequence similarity to the naphthalene-degrading, sulfate-reducing strain NaphS2. The anaerobic degradation pathway was studied by metabolite analyses and revealed phenanthroic acid as the major intermediate consistent with carboxylation as the initial activation reaction. Further reduced metabolites were indicative of a stepwise reduction of the ring system. We were able to measure the presumed second enzyme reaction in the pathway, phenanthroate-CoA ligase, in crude cell extracts. The reaction was specific for 2-phenanthroic acid and did not transform other isomers. The present study provides first insights into the anaerobic degradation pathways of three-ringed PAHs. The biochemical strategy follows principles known from anaerobic naphthalene degradation, including carboxylation and reduction of the aromatic ring system.

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Section: Discussionmentioning

confidence: 99%

Anaerobic degradation of phenanthrene by a sulfate‐reducing enrichment culture

Himmelberg

Brüls

Farmani

et al. 2018

Environmental Microbiology

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“…The genome of candidate Spirochaetaceae TRIP_4 suggests metabolic capacities similar to Rectinema cohabitans. The rodshape Spirochaete R. cohabitans was isolated from the naphthalene-degrading enrichment culture N47 where it is involved in necromass recycling providing hydrogen and possibly nutrients to the naphthalene-degrading Deltaproteobacterium N47 (Dong et al, 2018). Although the genetic elements for hydrogen transfer between the candidate Spirochaetaceae TRIP_4 and the candidate Desulfatiglans TRIP_1 are present, the corresponding gene products were not detected durig growth of the TRIP culture with phenanthrene.…”

Section: Resultsmentioning

confidence: 99%

“…The rodshape Spirochaete R. cohabitans was isolated from the naphthalene-degrading enrichment culture N47 where it is involved in necromass recycling providing hydrogen and possibly nutrients to the naphthalene-degrading Deltaproteobacterium N47 (Dong et al, 2018). A potential role in phenanthrene degradation of the four microorganisms other than candidate Desulfatiglans TRIP_1 could thus only be indirect.…”

Section: Amentioning

confidence: 99%

Metabolic reconstruction of the genome of candidate Desulfatiglans TRIP_1 and identification of key candidate enzymes for anaerobic phenanthrene degradation

Kraiselburd

Brüls

Heilmann

et al. 2019

Environmental Microbiology

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SummaryPolycyclic aromatic hydrocarbons (PAHs) are widely distributed pollutants. As oxygen is rapidly depleted in water‐saturated PAH‐contaminated sites, anaerobic microorganisms are crucial for their consumption. Here, we report the metabolic pathway for anaerobic degradation of phenanthrene by a sulfate‐reducing enrichment culture (TRIP) obtained from a natural asphalt lake. The dominant organism of this culture belongs to the Desulfobacteraceae family of Deltaproteobacteria and genome‐resolved metagenomics led to the reconstruction of its genome along with a handful of genomes from lower abundance bacteria. Proteogenomic analyses confirmed metabolic capabilities for dissimilatory sulfate reduction and indicated the presence of the Embden‐Meyerhof‐Parnas pathway, a complete tricarboxylic acid cycle as well as a complete Wood‐Ljungdahl pathway. Genes encoding enzymes putatively involved in the degradation of phenanthrene were identified. This includes two gene clusters encoding a multisubunit carboxylase complex likely involved in the activation of phenanthrene, as well as genes encoding reductases potentially involved in subsequent ring dearomatization and reduction steps. The predicted metabolic pathways were corroborated by transcriptome and proteome analyses, and provide the first insights into the metabolic pathway responsible for the anaerobic degradation of three‐ringed PAHs.

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“…In summary, migrated thermogenic hydrocarbons sustain diverse microbial populations in cold seep sediments in the deep seabed. These include key hydrocarbon degraders, syntrophic partners, and other community members, for example by recycling fermentation products and necromass of hydrocarbon degraders 20, 65 .…”

Section: Discussionmentioning

confidence: 99%

“…Desulfosarcina/Desulfococcus clade) 6 , and naphthalene (e.g. deltaproteobacterial strain NaphS2) 19, 20 . In parallel, culture-independent approaches have provided a holistic in situ perspective on hydrocarbon biodegradation, with most studies focused on hydrothermally influenced sediments that are rich in hydrocarbons 21–24 .…”

Section: Introductionmentioning

confidence: 99%

Thermogenic hydrocarbons fuel a redox stratified subseafloor microbiome in deep sea cold seep sediments

Dong

Rattray

Campbell

et al. 2020

Preprint

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20At marine cold seeps, gaseous and liquid hydrocarbons migrate from deep subsurface 21 origins to the sediment-water interface. Cold seep sediments are known to host 22CoM reductase pathway), longer-chain alkanes (fumarate addition pathway), and 35 aromatic hydrocarbons (fumarate addition and subsequent benzoyl-CoA pathways), 36 including novel lineages within Methanosarcinales and Chloroflexi. Geochemical 37 profiling demonstrated that hydrocarbon substrates are abundant in this location, 38 thermogenic in origin, and subject to biodegradation. The detection of alkyl-39 /arylalkylsuccinate metabolites, together with carbon isotopic signatures of ethane, 40propane and carbon dioxide, support that microorganisms are actively degrading 41 hydrocarbons in these sediments. Capacities for reductive dehalogenation, sulfide 42 oxidation, hydrogen oxidation, carbon fixation, and fermentation are also widespread. 43Most community members may indirectly benefit from thermogenic hydrocarbons 44 through interspecies transfer of electrons and metabolites, and degradation of 45 necromass. Thus, we conclude that upward migrated thermogenic hydrocarbons are 46 important carbon and energy sources that sustain diverse subseafloor microbial 47 communities at permanently cold hydrocarbon seeps. 48 3 Introduction 49 Marine cold seeps are characterised by the migration of gas and oil from deep 50 subsurface sources to the sediment-water interface 1, 2 . This seepage often contains 51 gaseous short-chain alkanes, as well as heavier liquid alkanes and aromatic 52 compounds 3 , that originate from deep thermogenic petroleum deposits. Migrated 53 hydrocarbons can serve as an abundant source of carbon and energy for 54 microorganisms in these ecosystems, either via their direct utilization or indirectly 55 through metabolizing by-products of hydrocarbon biodegradation 4 . Multiple 16S rRNA 56 gene surveys have revealed that cold seep sediments at or near the sediment-water 57 interface host an extensive diversity of archaeal and bacterial lineages 5-9 . However, 58 much less is known about metabolic versatility of this diverse microbiome, and how 59 surface and subsurface populations are connected and differentiated in different redox 60 zones within the sediment column 10, 11 . Most seep-associated microorganisms lack 61 sequenced genomes, precluding meaningful predictions of relationships between 62 microbial lineages and their biogeochemical functions 4, 8, 10-13 . 63 Geochemical studies have provided evidence that microorganisms in deep seafloor 64 sediments, including cold seeps, mediate anaerobic hydrocarbon oxidation 2, 3 . A range 65 of efforts have been undertaken to enrich and isolate anaerobic hydrocarbon-oxidizing 66 microorganisms from cold seep sediments and other ecosystems rich in hydrocarbons 67 (e.g. marine hydrothermal vents) [5][6][7][8][9] 14 . Numerous studies have focused on anaerobic 68 oxidation of methane, since methane generally is the dominant hydrocarbon in cold 69 seep fluids. This process is mediated by...

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Fermentative Spirochaetes mediate necromass recycling in anoxic hydrocarbon-contaminated habitats

Cited by 70 publications

References 57 publications

Anaerobic degradation of phenanthrene by a sulfate‐reducing enrichment culture

Anaerobic degradation of phenanthrene by a sulfate‐reducing enrichment culture

Metabolic reconstruction of the genome of candidate Desulfatiglans TRIP_1 and identification of key candidate enzymes for anaerobic phenanthrene degradation

Thermogenic hydrocarbons fuel a redox stratified subseafloor microbiome in deep sea cold seep sediments

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