The genome of Syntrophorhabdus aromaticivorans strain UI provides new insights for syntrophic aromatic compound metabolism and electron flow

Abstract

How aromatic compounds are degraded in various anaerobic ecosystems (e.g. groundwater, sediments, soils and wastewater) is currently poorly understood. Under methanogenic conditions (i.e. groundwater and wastewater treatment), syntrophic metabolizers are known to play an important role. This study explored the draft genome of Syntrophorhabdus aromaticivorans strain UI and identified the first syntrophic phenol-degrading phenylphosphate synthase (PpsAB) and phenylphosphate carboxylase (PpcABCD) and syntrophic terephthalate-degrading decarboxylase complexes. The strain UI genome also encodes benzoate degradation through hydration of the dienoyl-coenzyme A intermediate as observed in Geobacter metallireducens and Syntrophus aciditrophicus. Strain UI possesses electron transfer flavoproteins, hydrogenases and formate dehydrogenases essential for syntrophic metabolism. However, the biochemical mechanisms for electron transport between these H2 /formate-generating proteins and syntrophic substrate degradation remain unknown for many syntrophic metabolizers, including strain UI. Analysis of the strain UI genome revealed that heterodisulfide reductases (HdrABC), which are poorly understood electron transfer genes, may contribute to syntrophic H2 and formate generation. The genome analysis further identified a putative ion-translocating ferredoxin : NADH oxidoreductase (IfoAB) that may interact with HdrABC and dissimilatory sulfite reductase gamma subunit (DsrC) to perform novel electron transfer mechanisms associated with syntrophic metabolism.

Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor

“…These Pelotomaculum indeed encode and express genes for syntrophic energy conservation (Hdr-Ifo and ECHyd) and a previously observed pathway for TA degradation to acetate, CO 2 and H 2 (Figure 2 and Supplementary Table S4) (McInerney et al, 2007;Lykidis et al, 2011). In addition, we newly identify expression of a clostridial electron-bifurcating butyryl-CoA dehydrogenase in TAPelo3 that may facilitate the previously hypothesized Sporotomaculum-like energy-conserving butyrate generation from aromatic compound degradation (Qiu et al, 2003;Buckel and Thauer, 2013;Wu et al, 2013;Nobu et al, 2014), albeit refuting the involvement of previously identified non-energy-conserving acylCoA dehydrogenase (Lykidis et al, 2011;Wu et al, 2013). Although butyrate-fermenting TA degradation is thermodynamically more favorable, it sacrifices precious adenosine triphosphate from substrate-level phosphorylation.…”

“…Although its genome lacks the benzoate degradation pathway, we identify expression of Hdr-Ifo, ECHyd and FixABCX (Figures 2 and 3 and Supplementary Table S2), suggesting the capacity to syntrophically degrade carboxylates. In agreement, this organism expresses a butyrate degradation pathway similar to Syntrophomonas that also depends on identical energy conservation pathways (Supplementary Table S7; Sieber et al, 2010;Nobu et al, 2014). In addition, this clade expresses newly postulated syntrophic branched-chain fatty acid (that is, 2-methylbutyrate, isovalerate and isobutyrate) degradation pathways that are consistent with previous cultivation-based studies (Conrad et al, 1974;Stieb and Schink 1986;Matthies and Schink, 1992) and share high homology with other organisms thought to degrade branched-chain fatty acids (Supplementary Note, Supplementary Figure S5 and Supplementary Table S7).…”

“…In order to better understand energy-conserving mechanisms employed for acetogenesis and syntrophic metabolism, we survey all publically available homoacetogen and syntroph genomes (Supplementary Note). Many syntrophs appear to rely on the capacity to perform reverse electron transport-driven energy-conserving H 2 generation through electron-confurcating hydrogenase (ECHyd) in combination with reduced ferredoxin (Fd red )-generating Rhodobacter nitrogen fixation (Rnf) complex (Rnf; NADH:Fd oxidoreductase) or Hdr-Ifo (heterodisulfide-reductase-associated ion-translocating Fd:NADH oxidoreductase) (Sieber et al, 2012;Nobu et al, 2014). Specifically, the syntroph-characteristic co-occurrence of Hdr-Ifo and ECHyd can serve as a good indicator for syntrophic capacity.…”

“…Based on the known metabolic diversity of methanogenic environments (Schink, 1997;McInerney et al, 2009), uncultivated secondary degraders and scavengers must perform fermentative, syntrophic or acetogenic metabolism. To investigate the ecological roles and metabolic capabilities of the uncultivated taxa, this study used an 'ecogenomics' approach synthesizing single-cell genomics (Marcy et al, 2007), metagenomics (Tyson et al, 2004), metatranscriptomics (Frias-Lopez et al, 2008) and metabolic reconstruction assisted by comparative genomics of acetogen and syntroph energy conservation pathways (McInerney et al, 2007;Muller et al, 2008;Sieber et al, 2010Sieber et al, , 2012Nobu et al, 2014). In doing so, we provide the first look into the genomes and metabolism of many uncultivated taxa and propose how these organisms metabolically interact to achieve holistic carbon flux from TA to CH 4 and CO 2 in the methanogenic reactor.…”

Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics

“…In addition to the BMC, OP9-1 lineages appear to have other Fd-independent NADH sinks, such as NiFe hydrogenase and alcohol/aldehyde dehydrogenase . However, the putative propionate-oxidizing 'Atribacteria' lineages lack these enzymes as well as NADH:Fd oxidoreductases such as Rnf (Sieber et al, 2012;Nobu et al, 2015a) that syntrophic propionate oxidizers typically rely on to circumvent this issue. The only obvious alternative NADH sink encoded by the putative propionate-oxidizing JS1-1 and JS1-2 lineages involves acetyl-CoA reduction to acetaldehyde by BMC-associated PduPL (Figure 4a), suggesting that the BMC has a critical role in propionate catabolism.…”