Distribution of Extracellular Flavins in a Coastal Marine Basin and Their Relationship to Redox Gradients and Microbial Community Members

Abstract

The flavins (including flavin mononucleotide [FMN] and riboflavin [RF]) are a class of organic compounds synthesized by organisms to assist in critical redox reactions. While known to be secreted extracellularly by some species in laboratory-based cultures, flavin concentrations are largely unreported in the natural environment. Here, we present pore water and water column profiles of extracellular flavins (FMN and RF) and two degradation products (lumiflavin and lumichrome) from a coastal marine basin in the Southern California Bight alongside ancillary geochemical and 16S rRNA microbial community data. Flavins were detectable at picomolar concentrations in the water column (93-300 pM FMN, 14-40 pM RF) and low nanomolar concentrations in pore waters (250-2070 pM FMN, 11-210 pM RF). Elevated pore water flavin concentrations displayed an increasing trend with sediment depth and were significantly correlated with the total dissolved Fe (negative) and Mn (positive) concentrations. Network analysis revealed a positive relationship between flavins and the relative abundance of Dehalococcoidia and the MSBL9 clade of Planctomycetes, indicating possible secretion by members of these lineages. These results suggest that flavins are a common component of the so-called shared extracellular metabolite pool, especially in anoxic marine sediments where they exist at physiologicallyrelevant concentrations for metal oxide reduction.

Contrasting bacterial and archaeal distributions reflecting different geochemical processes in a sediment core from the Pearl River Estuary

“…Dissolved Mn showed positive correlations with four OTUs belonging to Desulfobacterales, Syntrophbacterales and Bathyarchaeota, while dissolved Fe was more closely related to OTUs that were affiliated to Dehalococcoidia, Anaerolineae and Planctomycetes. This result was different from the findings in San Pedro Basin (Monteverde et al 2018) where dissolved Fe exhibited close positive correlations with proteobacterial OTUs. Bacterial or archaeal OTUs showed few direct correlations with DOC and DIC, but were closely correlated to δ 13 C TOC and NH 4 + .…”

“…Bacterial groups such as Anaerolineaceae, Dehalococcoidia and Desulfarculales have been linked to the degradation of recalcitrant organic compounds (Oni et al 2015b). They were mainly present in the deep layers in previous studies (Monteverde et al 2018;Qiao et al 2018) and showed positive correlations with NH 4 + , δ 13 C TOC values and humic-like FDOM in this study (Fig. 5).…”

Microbial community and geochemical analyses of trans-trench sediments for understanding the roles of hadal environments

“…All three Chloroflexi OTUs were assigned to class Dehalococcoidia, which is frequently detected from seafloor sediments and possesses genes related to hydrogen and sulfur compound oxidation with reductive dehalogenation of halogenated organic compounds [88–90]. Notably, MSBL9 and Dehalococcoidia possess potential of flavin secretion in marine sediments [91], implying that these lineages also contribute to maintaining extracellular metabolite pools in hadal sediments. The single Bacteroidetes OTU was affiliated with class BD2-2, which may interact with methanotrophic archaea and sulfate-reducing bacteria in methane seep sediments [92].…”

Electroactive microorganisms in bioelectrochemical systems

“…Notably, Shewanella putrefaciens produced 4,400 mW m −2 with specially designed electrode materials 39 . In the environment, mediators such as flavins have been detected in marine sediments and pore waters, with the concentrations positively correlated to the concentrations of dissolved manganese, which suggests that the flavins might contribute to the reduction of insoluble manganese through extracellular electron transfer 40 .…”