Summary
Propionate is an important intermediate in the anaerobic mineralization of organic matter. In methanogenic environments, its degradation relies on syntrophic associations between syntrophic ...propionate‐oxidizing bacteria (SPOB) and Archaea. However, only 10 isolated species have been identified as SPOB so far. We report syntrophic propionate oxidation in thermophilic enrichments of Candidatus Syntrophosphaera thermopropionivorans, a novel representative of the candidate phylum Cloacimonetes. In enrichment culture, methane was produced from propionate, while Ca. S. thermopropionivorans contributed 63% to total bacterial cells. The draft genome of Ca. S. thermopropionivorans encodes genes for propionate oxidation via methymalonyl‐CoA. Phylogenetically, Ca. S. thermopropionivorans affiliates with the uncultured Cloacimonadaceae W5 and is more distantly related (86.4% 16S rRNA gene identity) to Ca. Cloacimonas acidaminovorans. Although Ca. S. thermopropionivorans was enriched from a thermophilic biogas reactor, Ca. Syntrophosphaera was in particular associated with mesophilic anaerobic digestion systems. 16S rRNA gene amplicon sequencng and a novel genus‐specific quantitative PCR assay consistently identified Ca. Syntrophosphaera/Cloacimonadaceae W5 in 9 of 12 tested full‐scale biogas reactors thereby outnumbering other SPOB such as Pelotomaculum, Smithella and Syntrophobacter. Taken together the ubiquity and abundance of Ca. Syntrophosphaera, those SPOB might be key players for syntrophic propionate metabolism that have been overlooked before.
Abstract
Sulfate-reducing microorganisms represent a globally important link between the sulfur and carbon cycles. Recent metagenomic surveys expanded the diversity of microorganisms putatively ...involved in sulfate reduction underscoring our incomplete understanding of this functional guild. Here, we use genome-centric metatranscriptomics to study the energy metabolism of
Acidobacteriota
that carry genes for dissimilation of sulfur compounds in a long-term continuous culture running under alternating anoxic and oxic conditions. Differential gene expression analysis reveals the unique metabolic flexibility of a pectin-degrading acidobacterium to switch from sulfate to oxygen reduction when shifting from anoxic to oxic conditions. The combination of facultative anaerobiosis and polysaccharide degradation expands the metabolic versatility among sulfate-reducing microorganisms. Our results highlight that sulfate reduction and aerobic respiration are not mutually exclusive in the same organism, sulfate reducers can mineralize organic polymers, and anaerobic mineralization of complex organic matter is not necessarily a multi-step process involving different microbial guilds but can be bypassed by a single microbial species.
Anaerobic digestion (AD) is a globally important technology for effective waste and wastewater management. In AD, microorganisms interact in a complex food web for the production of biogas. Here, ...acetoclastic methanogens and syntrophic acetate-oxidizing bacteria (SAOB) compete for acetate, a major intermediate in the mineralization of organic matter. Although evidence is emerging that syntrophic acetate oxidation is an important pathway for methane production, knowledge about the SAOB is still very limited.
A metabolic reconstruction of metagenome-assembled genomes (MAGs) from a thermophilic solid state biowaste digester covered the basic functions of the biogas microbial community. Firmicutes was the most abundant phylum in the metagenome (53%) harboring species that take place in various functions ranging from the hydrolysis of polymers to syntrophic acetate oxidation. The Wood-Ljungdahl pathway for syntrophic acetate oxidation and corresponding genes for energy conservation were identified in a Dethiobacteraceae MAG that is phylogenetically related to known SAOB. 16S rRNA gene amplicon sequencing and enrichment cultivation consistently identified the uncultured Dethiobacteraceae together with Syntrophaceticus, Tepidanaerobacter, and unclassified Clostridia as members of a potential acetate-oxidizing core community in nine full-scare digesters, whereas acetoclastic methanogens were barely detected.
Results presented here provide new insights into a remarkable anaerobic digestion ecosystem where acetate catabolism is mainly realized by Bacteria. Metagenomics and enrichment cultivation revealed a core community of diverse and novel uncultured acetate-oxidizing bacteria and point to a particular niche for them in dry fermentation of biowaste. Their genomic repertoire suggests metabolic plasticity besides the potential for syntrophic acetate oxidation. Video Abstract.
To date, very little is known about the bacterial core community of marine sediments. Here we study the environmental distribution, abundance and ecogenomics of the gammaproteobacterial ...Woeseiaceae/JTB255 marine benthic group. A meta-analysis of published work shows that the Woeseiaceae/JTB255 are ubiquitous and consistently rank among the most abundant 16S rRNA gene sequences in diverse marine sediments. They account for up to 22% of bacterial amplicons and 6% of total cell counts in European and Australian coastal sediments. The analysis of a single-cell genome, metagenomic bins and the genome of the next cultured relative Woeseia oceani indicated a broad physiological range, including heterotrophy and facultative autotrophy. All tested (meta)genomes encode a truncated denitrification pathway to nitrous oxide. The broad range of energy-yielding metabolisms possibly explains the ubiquity and high abundance of Woeseiaceae/JTB255 in marine sediments, where they carry out diverse, but yet unknown ecological functions.
Marine sediments are the largest carbon sink on earth. Nearly half of dark carbon fixation in the oceans occurs in coastal sediments, but the microorganisms responsible are largely unknown. By ...integrating the 16S rRNA approach, single-cell genomics, metagenomics and transcriptomics with (14)C-carbon assimilation experiments, we show that uncultured Gammaproteobacteria account for 70-86% of dark carbon fixation in coastal sediments. First, we surveyed the bacterial 16S rRNA gene diversity of 13 tidal and sublittoral sediments across Europe and Australia to identify ubiquitous core groups of Gammaproteobacteria mainly affiliating with sulfur-oxidizing bacteria. These also accounted for a substantial fraction of the microbial community in anoxic, 490-cm-deep subsurface sediments. We then quantified dark carbon fixation by scintillography of specific microbial populations extracted and flow-sorted from sediments that were short-term incubated with (14)C-bicarbonate. We identified three distinct gammaproteobacterial clades covering diversity ranges on family to order level (the Acidiferrobacter, JTB255 and SSr clades) that made up >50% of dark carbon fixation in a tidal sediment. Consistent with these activity measurements, environmental transcripts of sulfur oxidation and carbon fixation genes mainly affiliated with those of sulfur-oxidizing Gammaproteobacteria. The co-localization of key genes of sulfur and hydrogen oxidation pathways and their expression in genomes of uncultured Gammaproteobacteria illustrates an unknown metabolic plasticity for sulfur oxidizers in marine sediments. Given their global distribution and high abundance, we propose that a stable assemblage of metabolically flexible Gammaproteobacteria drives important parts of marine carbon and sulfur cycles.
Acetate is a key intermediate in anaerobic mineralization of organic matter in marine sediments. Its turnover is central to carbon cycling, however, the relative contribution of different microbial ...populations to acetate assimilation in marine sediments is unknown. To quantify acetate assimilation by
abundant bacterial populations, we incubated coastal marine sediments with
C-labeled acetate and flow-sorted cells that had been labeled and identified by fluorescence
hybridization. Subsequently, scintillography determined the amount of
C-acetate assimilated by distinct populations. This approach fostered a high-throughput quantification of acetate assimilation by phylogenetically identified populations. Acetate uptake was highest in the oxic-suboxic surface layer for all sorted bacterial populations, including deltaproteobacterial sulfate-reducing bacteria (SRB), which accounted for up to 32% of total bacterial acetate assimilation. We show that the family
also assimilates acetate in marine sediments, while the more abundant
dominated acetate assimilation despite lower uptake rates. Unexpectedly, members of
accounted for the highest relative acetate assimilation in all sediment layers with up to 31-62% of total bacterial acetate uptake. We also show that acetate is used to build up storage compounds such as polyalkanoates. Together, our findings demonstrate that not only the usual suspects SRB but a diverse bacterial community may substantially contribute to acetate assimilation in marine sediments. This study highlights the importance of quantitative approaches to reveal the roles of distinct microbial populations in acetate turnover.
Summary
Zero‐valence sulfur (S0) is a central intermediate in the marine sulfur cycle and forms conspicuous accumulations at sediment surfaces, hydrothermal vents and in oxygen minimum zones. Diverse ...microorganisms can utilize S0, but those consuming S0 in the environment are largely unknown. We identified possible key players in S0 turnover on native or introduced S0 in benthic coastal and deep‐sea habitats using the 16S ribosomal RNA approach, (in situ) growth experiments and activity measurements. In all habitats, the epsilonproteobacterial Sulfurimonas/Sulfurovum group accounted for a substantial fraction of the microbial community. Deltaproteobacterial Desulfobulbaceae and Desulfuromonadales were also frequently detected, indicating S0 disproportionation and S0 respiration under anoxic conditions. Sulfate production from S0 particles colonized in situ with Sulfurimonas/Sulfurovum suggested that this group oxidized S0. We also show that the type strain Sulfurimonas denitrificans is able to access cyclooctasulfur (S8), a metabolic feature not yet demonstrated for sulfur oxidizers. The ability to oxidize S0, in particular S8, likely facilitates niche partitioning among sulfur oxidizers in habitats with intense microbial sulfur cycling such as sulfidic sediment surfaces. Our results underscore the previously overlooked but central role of Sulfurimonas/Sulfurovum group for conversion of free S0 at the seafloor surface.
Summary
Anaerobic digestion (AD) is an important technology for the effective conversion of waste and wastewater to methane. Here, syntrophic bacteria transfer molecular hydrogen (H2), formate, or ...directly supply electrons (direct interspecies electron transfer, DIET) to the methanogens. Evidence is accumulating that the methanation of short‐chain fatty acids can be enhanced by the addition of conductive material to the anaerobic digester, which has often been attributed to the stimulation of DIET. Since little is known about the transcriptional response of a complex AD microbial community to the addition of conductive material, we added magnetite to propionate‐fed laboratory‐scale reactors that were inoculated with wastewater sludge. Compared to the control reactors, the magnetite‐amended reactors showed improved methanation of propionate. A genome‐centric metatranscriptomics approach identified the active SCFA‐oxidizing bacteria that affiliated with Firmicutes, Desulfobacterota and Cloacimonadota. The transcriptional profiles revealed that the syntrophic bacteria transferred acetate, H2 and formate to acetoclastic and hydrogenotrophic methanogens, whereas transcription of potential determinants for DIET such as conductive pili and outer‐membrane cytochromes did not significantly change with magnetite addition. Overall, changes in the transcriptional profiles of syntrophic Bacteria and Archaea in propionate‐fed lab‐scale reactors amended with magnetite refute a major role of DIET in the studied system.
Molecular hydrogen (H
) is the key intermediate in the anaerobic degradation of organic matter. Its removal by H
-oxidizing microorganisms is essential to keep anaerobic degradation energetically ...favourable. Sulfate-reducing microorganisms (SRM) are known as the main H
scavengers in anoxic marine sediments. Although the community of marine SRM has been extensively studied, those consuming H
in situ are completely unknown. We combined metagenomics, PCR-based clone libraries, single-amplified genomes (SAGs) and metatranscriptomics to identify potentially H
-consuming SRM in anoxic coastal sediments. The vast majority of SRM-related H
ase sequences were assigned to group 1b and 1c NiFe-H
ases of the deltaproteobacterial order Desulfobacterales. Surprisingly, the same sequence types were similarly highly expressed in spring and summer, suggesting that these are stable and integral members of the H
-consuming community. Notably, one sequence cluster from the SRM group 1 consistently accounted for around half of all NiFe-H
ase transcripts. Using SAGs, we could link this cluster with the 16S rRNA genes of the uncultured Sva0081-group of the family Desulfobacteraceae. Sequencing of 16S rRNA gene amplicons and H
ase gene libraries suggested consistently high in situ abundance of the Sva0081 group also in other marine sediments. Together with other Desulfobacterales these likely are important H
-scavengers in marine sediments.
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