Genomic Insights into the Carbon and Energy Metabolism of a Thermophilic Deep-Sea Bacterium Deferribacter autotrophicus Revealed New Metabolic Traits in the Phylum Deferribacteres

Abstract

Information on the biochemical pathways of carbon and energy metabolism in representatives of the deep lineage bacterial phylum Deferribacteres are scarce. Here, we report the results of the sequencing and analysis of the high-quality draft genome of the thermophilic chemolithoautotrophic anaerobe Deferribacter autotrophicus. Genomic data suggest that CO2 assimilation is carried out by recently proposed reversible tricarboxylic acid cycle (“roTCA cycle”). The predicted genomic ability of D. autotrophicus to grow due to the oxidation of carbon monoxide was experimentally proven. CO oxidation was coupled with the reduction of nitrate to ammonium. Utilization of CO most likely involves anaerobic [Ni, Fe]-containing CO dehydrogenase. This is the first evidence of CO oxidation in the phylum Deferribacteres. The genome of D. autotrophicus encodes a Nap-type complex of nitrate reduction. However, the conversion of produced nitrite to ammonium proceeds via a non-canonical pathway with the participation of hydroxylamine oxidoreductase (Hao) and hydroxylamine reductase. The genome contains 17 genes of putative multiheme c-type cytochromes and “e-pilin” genes, some of which are probably involved in Fe(III) reduction. Genomic analysis indicates that the roTCA cycle of CO2 fixation and putative Hao-enabled ammonification may occur in several members of the phylum Deferribacteres.

Metagenomic Investigation of a Low Diversity, High Salinity Offshore Oil Reservoir

“…Arhodomonas aquaeolei (MAG 2) is known to reduce nitrate but not nitrite [44], consistent with narGHI genes being identified within the genome of MAG 2 (Figure 3). This Nar gene complex was also found in the genome of Flexistipes sinusarabici (MAG 5), contrary to another study of a different member of this species [58]. The same complex was also found within Geotoga (MAG 9), consistent with Geotoga spp.…”

“…In this reservoir, Geotoga petrae (MAG 9) is shown to contain these DNRA genes. In addition to the Nar complex, napA (nitrate reductase cytochrome; Figure 3) was identified in Arhodomonas (MAG 2) and Flexistipes (MAG 5) genomes, as demonstrated previously in Flexistipes sinusarabici [58]. Arhodomonas aquaeolei (MAG 2) and Geotoga petraea (MAG 9) contain the nirBD and nrfAH genes involved in the reduction of nitrite to ammonia, the second step in DNRA (Figure 3).…”

“…Reduction of thiosulfate to sulfide can be mediated by phsABC (Figure 2), which were found within the genomes of Flexistipes sinusarabici (MAG 5) and Geotoga petraea (MAG 9). Sulfide production by members of both of these genera has been reported previously [43,58]. Halanaerobium congolense is also a thiosulfate and elemental sulfur respiring organism [48]; however, associated genes were not detected in closely related MAG 6, possibly due to its low genome completeness (59%; Table 1).…”

Genome analysis of Thermosulfuriphilus ammonigenes ST65T, an anaerobic thermophilic chemolithoautotrophic bacterium isolated from a deep-sea hydrothermal vent

“…Yet, the genome of strain ST65 T contains genes of hydroxylamine oxidoreductases (Hao) and hydroxylamine reductase (Hcp). Thus, the Nrf complex in T. ammonigenes could be replaced by an ammonification pathway based on Hao and Hcp enzymes as it has been proposed for several other marine bacteria (Hanson et al, 2013;Slobodkina et al, 2017a;Slobodkin et al, 2019). Sulfur cycle is of a great importance in the deep-sea environments.…”

Biome-specific distribution of Ni-containing carbon monoxide dehydrogenases

“…Because of the low redox potential of CO ( E 0′ = − 520 mV), the coupling of CO oxidation and H + reduction is undertaken by the Ni-CODH/electron carrier polyferredoxin CooF/energy converting hydrogenase (ECH) respiratory complex, which is an ancient respiratory module (Soboh et al 2002 ; Singer et al 2006 ; Schoelmerich and Müller 2019 ). In addition, Ni-CODH associated with flavin adenine dinucleotide-dependent NAD(P) oxidoreductase (FNOR) and CooF is considered to enable NAD(P)H-mediated CO-driven respiration (Whitham et al 2015 ; Geelhoed et al 2016 ; Slobodkin et al 2019 ).…”