Dual Role of Humic Substances As Electron Donor and Shuttle for Dissimilatory Iron Reduction

Dissimilatory iron-reducing bacteria (DIRB) are known to use humic substances (HS) as electron shuttles for dissimilatory iron reduction (DIR) by transferring electrons to HS-quinone moieties, which in turn rapidly reduce Fe­(III) oxides. However, the potential for HS to serve as a source of organic carbon (OC) that can donate electrons for DIR is unknown. We studied whether humic acids (HA) and humins (HM) recovered from peat soil by sodium pyrophosphate extraction could serve as both electron shuttles and electron donors for DIR by freshwater sediment microorganisms. Both HA and HM served as electron shuttles in cultures amended with glucose. However, only HA served as an electron donor for DIR. Metagenomes from HA-containing cultures had an overrepresentation of genes involved in polysaccharide and to a lesser extent aromatic compound degradation, suggesting complex OC metabolism. Genomic searches for the porin-cytochrome complex involved in DIR resulted in matches to <i>Ignavibacterium/Melioribacter</i>, DIRB capable of polymeric OC metabolism. These results indicate that such taxa may have played a role in both DIR and decomposition of complex OC. Our results suggest that decomposition of HS coupled to DIR and other anaerobic pathways could play an important role in soil and sediment OC metabolism

Inventory of putative glycoside hydrolases (GHs) in plant cell wall degradation in termite hindguts and other environments^a.

a<p>The listed value is the population abundance weighted relative abundance (%) of GH families among the total GHs included in the table used in Allgaier <i>et al</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061126#pone.0061126-Allgaier1" target="_blank">[28]</a>.</p>b<p>An improved version of assembly was used, leading to subtle differences in numbers from originally reported by Warnecke <i>et al</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061126#pone.0061126-Warnecke1" target="_blank">[6]</a>.</p>c<p>Percentages of GHs were directly from Allgaier <i>et al</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061126#pone.0061126-Allgaier1" target="_blank">[28]</a>.</p>d<p>GH gene counts were from Pope <i>et al</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061126#pone.0061126-Pope1" target="_blank">[29]</a>and the percentages were renormalized by total number of GHs included in the table used in Allgaier <i>et al</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061126#pone.0061126-Allgaier1" target="_blank">[28]</a>, for comparison among these studies.</p>e<p>Percentages were calculated based on GH gene counts reported in Brulc <i>et al</i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0061126#pone.0061126-Brulc1" target="_blank">[31]</a>.</p>f<p>No pfam domain is available and the identification is performed by BLAST search.</p>g<p>GHs over- (^**) or under-represented (^*) in <i>A. wheeleri</i> compared to the laboratory <i>N. corniger</i> (after adjusting for multiple hypothesis test, with a false discovery rate P-value cutoff of 0.05), and the difference was supported by the comparison between <i>A. wheeleri</i> and Costa Rican <i>Nasutitermes</i> sp.. The comparison was based on GH abundances normalized by the total abundance of GHs listed in this table.</p

Taxonomic assignment of nickel-iron (NiFe) hydrogenases (a), the large subunit of iron-only (FeFe) hydrogenases (b), formyl tetrahydrofolate synthase (FTHFS) (c), and glycoside hydrolases family 3 (GH3) (d) by MEGAN using Blastp results against the NR database.

<p>Taxonomic assignment of nickel-iron (NiFe) hydrogenases (a), the large subunit of iron-only (FeFe) hydrogenases (b), formyl tetrahydrofolate synthase (FTHFS) (c), and glycoside hydrolases family 3 (GH3) (d) by MEGAN using Blastp results against the NR database.</p

Phylogenetic affiliation, relative abundance and habitat distribution of OTUs that are >0.5% of total bacterial community.

<p>The bubble size represents the relative abundance of each OTU, and bubble color indicates the types of habitats where their closest relatives in the greengenes database were found. OTUs marked red were exclusively found in higher termites, orange OTUs were restricted to termites, including both higher and lower termites, green OTUs were also found in the guts and feces of other animals (e.g. cow, goat and elephant). Blue OTUs were found in other anoxic environments, such as anaerobic digesters.</p

Key metabolic differences between cow dung- and wood-feeding termites based on gene and transcript abundance profiles.

<p>In this schematic summary, intracellular and extracellular reactions are separated by a cell membrane, but these reactions do not necessarily all occur in one cell. Green or red thin lines (including rectangle outlines) indicate genes more abundant in the <i>A. wheeleri</i> or <i>N. corniger</i> metagenome, respectively. Green or red thick lines (including rectangle highlights) indicate transcripts more abundant in the <i>A. wheeleri</i> or <i>N. corniger</i> metatranscriptome, respectively. Black lines indicate equal representation in both termite genera.</p