High biodiversity in a benzene-degrading nitrate-reducing culture is sustained by a few primary consumers

Abstract

A key question in microbial ecology is what the driving forces behind the persistence of large biodiversity in natural environments are. We studied a microbial community with more than 100 different types of species which evolved in a 15-years old bioreactor with benzene as the main carbon and energy source and nitrate as the electron acceptor. Using genome-centric metagenomics plus metatranscriptomics, we demonstrate that most of the community members likely feed on metabolic left-overs or on necromass while only a few of them, from families Rhodocyclaceae and Peptococcaceae, are candidates to degrade benzene. We verify with an additional succession experiment using metabolomics and metabarcoding that these few community members are the actual drivers of benzene degradation. As such, we hypothesize that high species richness is maintained and the complexity of a natural community is stabilized in a controlled environment by the interdependencies between the few benzene degraders and the rest of the community members, ultimately resulting in a food web with different trophic levels.

Structure and functional capacity of a benzene-mineralizing, nitrate-reducing microbial community

“…Microbial community analyses indicated that a distinct member of the Peptococcaceae was growing while oxidizing benzene and other members of the community became also slightly enriched suggesting that benzene was mineralized by syntrophic interactions of the primary benzene degrader with nitrate reducers. Similar communities have been reported by others (Atashgahi et al, 2018; Kunapuli et al, 2007; Luo et al, 2016; Melkonian et al, 2021), but the initial degrader observed in this study is phylogenetically distinct from other putative benzene degraders indicating a broad diversity of anaerobic benzene degraders within the Peptococcaceae . In addition, benzene was likely initially carboxylated as indicated by metaproteomic detection of subunit AbcA of the putative benzene carboxlyase; this protein has always been detected in benzene‐degrading Peptococcaceae ‐dominated cultures to date.…”

“…Furthermore, we detected a UbiX‐like carboxylase 64.4% similar to a putative UbiX‐like carboxylase in the same benzene‐degrading culture BF (Table 2). The involvement of abc genes related to Peptococcaceae in benzene carboxylation under nitrate‐reducing conditions was reported in recent studies (Atashgahi et al, 2018; Luo et al, 2014; Melkonian et al, 2021; Toth et al, 2021); hence the results of these studies together with our data strongly suggest that carboxylation by Peptococcaceae is a common activation mechanism for benzene degradation under nitrate‐reducing conditions.…”

“…Notably, the concurrent transcription of genes encoding enzymes catalysing oxygen-dependent benzene hydroxylation was also observed during benzene degradation under nitrate-reducing conditions (Atashgahi et al, 2018;Melkonian et al, 2021), suggesting either oxygen contamination or the presence of molecular oxygen possibly formed via nitric oxide dismutase as proposed for methane or alkane oxidizers under nitrate-reducing conditions (Ettwig et al, 2010;Zedelius et al, 2011).…”

Characterization of growth and development of sorghum genotypes with differential susceptibility to Striga hermonthica

“…Samples were centrifuged at 7600 relative centrifugal force at 10 °C for 5 min, and the supernatant was collected and filtered through a 0.22 µm-pore filter. Metabolite analysis by LC-MS was carried out as described in Melkonian et al (2021) with slight modifications. Five microliters of root extract was injected in a Nexera ultra-high performance liquid chromatography (UHPLC) system (Shimadzu, Den Bosch, The Netherlands) coupled to a high-resolution quadrupole time-of-flight mass spectrometer (Q-TOF; maXis 4G, Bruker Daltonics, Bruynvisweg 16/18).…”

Transient Oxygen Exposure Causes Profound and Lasting Changes to a Benzene-Degrading Methanogenic Community

“…Nealsonbacteria (OD1) and Ca . Omnitrophica (OP3), among others, are periodically observed in high abundances in the DGG-B/OR consortium (Luo et al, 2016; Toth et al, 2021) and other anaerobic benzene-degrading consortia (Taubert et al, 2012; Melkonian et al, 2021). What factors could explain such relatively high decay rates?…”