An Ecological Basis for Dual Genetic Code Expansion in Marine Deltaproteobacteria

Abstract

Marine benthic environments may be shaped by anthropogenic and other localized events, leading to changes in microbial community composition evident decades after a disturbance. Marine sediments in particular harbor exceptional taxonomic diversity and can shed light on distinctive evolutionary strategies. Genetic code expansion is a strategy that increases the structural and functional diversity of proteins in cells, by repurposing stop codons to encode non-canonical amino acids: pyrrolysine (Pyl) and selenocysteine (Sec). Here, we report both a study of the microbiome at a deep sea industrial waste dumpsite and an unanticipated discovery of codon reassignment in its most abundant member, with potential ramifications for interpreting microbial interactions with ocean-dumped wastes. The genomes of abundant Deltaproteobacteria from the sediments of a deep-ocean chemical waste dump site have undergone genetic code expansion. Pyl and Sec in these organisms appear to augment trimethylamine (TMA) and one-carbon metabolism, representing an increased metabolic versatility. The inferred metabolism of these sulfate-reducing bacteria places them in competition with methylotrophic methanogens for TMA, a contention further supported by earlier isotope tracer studies and reanalysis of metatranscriptomic studies. A survey of genomic data further reveals a broad geographic distribution of a niche group of similarly specialized Deltaproteobacteria, including at sulfidic sites in the Atlantic Ocean, Gulf of Mexico, Guaymas Basin, and North Sea, as well as in terrestrial and estuarine environments. These findings reveal an important biogeochemical role for specialized Deltaproteobacteria at the interface of the carbon, nitrogen, selenium, and sulfur cycles, with their niche adaptation and ecological success potentially augmented by genetic code expansion.

Evidence of cryptic methane cycling and non-methanogenic methylamine consumption in the sulfate-reducing zone of sediment in the Santa Barbara Basin, California

“…This finding further suggests a competition between methanogens and sulfate-reducing bacteria for methylamine; however, the authors could not rule out AOM as a potential contributor to the inorganic carbon pool. Kivenson et al (2021) discovered dual genetic code expansion in sulfate-reducing bacteria from sediment within a deep-sea industrial waste dumpsite in the San Pedro Basin, California, which potentially allows the metabolization of trimethylamine. The authors expanded their study to revisit metagenomic and metatranscriptomic data collected from the Baltic Sea and in the Columbia River estuary and found expression of trimethylamine methyltransferase in Deltaproteobacteria.…”

Selenium Metabolism and Selenoproteins in Prokaryotes: A Bioinformatics Perspective

“…Except sea water, the use of Sec in marine sediment microbiome was also investigated based on the metagenomic data from the sediments of a deep-ocean industrial waste dump site [ 87 ]. By analyzing the reconstructed genomes of Deltaproteobacteria, which are the most abundant mat organisms in the sediments, more than 30 putative selenoprotein genes (including both previously reported and newly predicted) were found, indicating a highly active utilization of Sec in the dominant deltaproteobacteria in marine sediments.…”

Anaerobic microbiology of methylated compounds in Black Sea sediments

“…Here, we have demonstrated the utilization of a range of methylated compounds by a new methylotrophic Desulfosporosinus nitroreducens strain P130 isolated from Black Sea sediments. Despite the genomic potential for methylotrophy of many marine SRM including D. nitroreducens strains 59.4B T and 59.4F, little in-depth inquiry into the genomic and physiological capabilities of anaerobic marine bacterial methylotrophy has been conducted so far, and most research has focused on the interplay between bacteria and methanogenic archaea or the general patterns of the degradation of methylated compounds (198,245,326,327). Both Black Sea sediment enrichments S5 and S29 with methanol as the only ubiquitous electron donor became dominated over time by one organism when methanogenesis was inhibited, as evidenced by reads per basepairs of the metagenome sequencing attributed to these specific MAGs.…”

“…However, in the genomes of putative sulfate-reducing Desulfobacterota, pyrrolysine biosynthesis coding genes were identified in marine sediments contaminated with industrial waste. This indicates that depending on environmental conditions, sulfate reduction may also be linked with the utilization of pyrrolysine (245).…”

“…In methanogens, the genetic code is adapted to the inclusion of pyrrolysine by minimizing TAG as stop codon in the genome to ~5%, whereas Acetohalobium arabaticum alters the biosynthesis of pyrrolysine and subsequent incorporation in the amino acid alphabet in the presence or absence of TMA (243). Furthermore, the genetic presence of TMA utilization coding genes has been explored in the human gut pathogen genus Bilophila and in marine Desulfobacterota although physiological data is lacking (245,324).…”