New Results

Novel insights into the taxonomic diversity and molecular mechanisms of bacterial Mn(III) reduction

Nadia Szeinbaum, Brook L. Nunn, Amanda R. Cavazos, Sean A. Crowe, Frank J. Stewart, Thomas J. DiChristina, Christopher T. Reinhard, Jennifer B. Glass
doi: https://doi.org/10.1101/695007

Summary

Soluble ligand-bound Mn(III) can support anaerobic microbial respiration in diverse aquatic environments. Thus far, Mn(III) reduction has only been associated with certain Gammaproteobacteria. Here, we characterized microbial communities enriched from Mn-replete sediments of Lake Matano, Indonesia. Our results provide the first evidence for biological reduction of soluble Mn(III) outside Gammaproteobacteria. Metagenome assembly and binning revealed a novel betaproteobacterium, which we designate “Candidatus Dechloromonas occultata.” This organism dominated the enrichment and expressed a porin-cytochrome c complex typically associated with iron-oxidizing Betaproteobacteria and a novel cytochrome c-rich protein cluster (Occ), including an undecaheme putatively involved in extracellular electron transfer. The occ gene cluster was detected in diverse aquatic bacteria, including uncultivated Betaproteobacteria from the deep subsurface. These observations provide new insight into the taxonomic and functional diversity of microbially-driven Mn(III) reduction in natural environments.

Originality-significance Statement The prevalence of Mn(III)-ligand complexes in diverse aquatic environments is a recent geochemical discovery. Thus far, microbially-driven Mn(III) reduction has only been associated with Gammaproteobacteria encoding three-component outer-membrane porin-cytochrome c conduits. Here, we demonstrate that Betaproteobacteria dominate in abundance and protein expression during Mn(III) reduction in an enrichment culture. Using metaproteomics, we detect for the first time that Betaproteobacteria express a two-component porin-cytochrome c conduit, and an uncharacterized extracellular undecaheme c-type cytochrome. Although undecahemes have never been reported in Betaproteobacteria, we find that they are widespread in uncultivated strains. These results widen the phylogenetic diversity of Mn(III)-reducing bacteria, and provide new insights into potential molecular mechanisms for soluble Mn(III) reduction.

Introduction

Manganese(III) is a strong oxidant with a reduction potential close to molecular oxygen (Kostka et al., 1995). Ligand-bound Mn(III) is often the most abundant dissolved Mn species in sediment porewaters (Madison et al., 2013; Oldham et al., 2019) and soils (Heintze and Mann, 1947). In the deep subsurface, microbes may rely on simple electron and carbon sources such as CH4, and metal oxide electron acceptors like Mn(III), to fuel anaerobic respiration (Beal et al., 2009). Manganese reduction coupled to CH4 oxidation is a thermodynamically favorable metabolism, and its natural occurrence is supported by biological and geochemical evidence (Crowe et al., 2011; Riedinger et al., 2014). Despite clear evidence for the environmental importance of Mn(III), knowledge about microbial Mn(III) cycling pathways remain fragmentary.

To date, only Shewanella spp. (Gammaproteobacteria) have been confirmed to respire soluble Mn(III) (Kostka et al., 1995; Szeinbaum et al., 2014). Shewanella respire Mn(III) using the Mtr pathway (Szeinbaum et al., 2017), a porin-cytochrome (PCC) conduit that transports electrons across the periplasm for extracellular respiration of Mn(III/IV), Fe(III), and other metals (Richardson et al., 2012; Shi et al., 2016). Many Fe(II)-oxidizing Betaproteobacteria also contain PCCs (MtoAB, generally lacking the C subunit), which are proposed to oxidize Fe(II) to Fe(III) by running the PCC in reverse (Emerson et al., 2013; Kato et al., 2015; He et al., 2017).

In some metal-reducing Gammaproteobacteria and Deltaproteobacteria, extracellular undecaheme (11-heme) UndA is thought to play a key functional role in soluble Fe(III) reduction (Fredrickson et al., 2008; Shi et al., 2011; Smith et al., 2013; Yang et al., 2013). UndA’s crystal structure shows a surface-exposed heme surrounded by positive charges, which may bind negatively-charged soluble iron chelates (Edwards et al., 2012).

Environmental omics suggests that metal reduction by Betaproteobacteria may be widespread in the deep subsurface (Anantharaman et al., 2016; Hernsdorf et al., 2017). However, only a few Fe(III)-reducing Betaproteobacteria isolates have been characterized (Cummings et al., 1999; Finneran et al., 2003), and little is known about metal reduction pathways in Betaproteobacteria. Here, we explored microbial Mn(III) reduction in enrichments inoculated with sediment from Lake Matano, Indonesia, which has active microbial Mn and methane (CH4) cycles (Jones et al., 2011). Our results provide the first evidence for biological reduction of soluble Mn(III) outside Gammaproteobacteria.

Results and discussion

Enrichment of Mn(III)-reducing populations

We designed an enrichment strategy to select for microbes capable of anaerobic CH4 oxidation coupled to soluble Mn(III) reduction by incubating anoxic Lake Matano communities with soluble Mn(III)-pyrophosphate as the electron acceptor (with 2% O2 in a subset of bottles), and CH4 as the sole electron donor and carbon source (see Supporting Information for enrichment details). Cultures were transferred into fresh media after Mn(III) was completely reduced to Mn(II), for a total of five transfers over 395 days. By the fourth transfer, cultures with CH4 headspace (with or without 2% O2) reduced ~80% of soluble Mn(III) compared to ~30% with N2 headspace (Fig. 1). 16S rRNA gene sequences were dominated by Betaproteobacteria (Rhodocyclales) and Deltaproteobacteria (Desulfuromonadales; Fig. S1). 13CH4 oxidation to 13CO2 was undetectable (Fig. S2).

Figure 1.
Figure 1. Consumption of Mn(III) in Lake Matano enrichments in the presence and absence of methane.

Sediment-free cultures (transfer 4) from 335 days after the initial enrichment were incubated for 45 days with 1 mM Mn(III) pyrophosphate as the sole electron acceptor. Initial bottle headspace contained 50% CH4 + 50% N2 (black circles), 50% CH4+48% N2+2% O2 (gray circles), 100% N2 (white circles), and 50% CH4+50% N2 heat killed controls (black triangles). Error bars are standard deviations from duplicate experiments. Color change from red to clear indicates Mn(III) reduction.

Samples for metagenomic and metaproteomic analysis were harvested from the fifth transfer (Fig. 1; Fig. S1). Out of 2,952 proteins identified in the proteome, 90%were assigned to Betaproteobacteria; of those, 72% mapped to a 99.5% complete metagenome-assembled genome (MAG; Rhodocyclales bacterium GT-UBC; NCBI accession QXPY01000000) with 81-82% average nucleotide identity (ANI) and phylogenetic affiliation to Dechloromonas spp. (Table S1; Fig. S3). This MAG is named here “Candidatus Dechloromonas occultata” sp. nov.; etymology: occultata; (L. fem. adj. ‘hidden’). The remaining 10% of proteins mapped to Deltaproteobacteria; of those, 70% mapped to a nearly complete MAG (Desulfuromonadales bacterium GT-UBC; NCBI accession RHLS01000000) with 80% ANI to Geobacter sulfurreducens. This MAG is named here “Candidatus Geobacter occultata”.

Cytochrome expression during Mn(III) reduction

Cytochromes containing multiple c-type hemes are key for electron transport during microbial metal transformations, and therefore might also be expected to play a role in Mn(III) reduction. Numerous mono-, di-, and multi (>3)-heme cytochromes (MHCs) were expressed by “Ca. D. occultata” in Mn(III)-reducing cultures. Nine out of 15 MHCs encoded by the “Ca. D. occultata” MAG were expressed, including two decahemes similar to MtoA in Fe(II)-oxidizing Betaproteobacteria (Tables 1, S2, S3; Figs. 2A, S4). Several highly expressed MHCs were encoded on a previously unreported 19-gene cluster with 10 cytochrome-c proteins, hereafter occA-S (Table 1; Figs. 2B, S5, S6). OccP was predicted to be an extracellular undecaheme protein of ~100 kDa (922 amino acids). “Ca. Dechloromonas occultata” may reduce Mn(III) using the novel extracellular undecaheme OccP as the terminal Mn(III) reductase. Experimental verification of the function of the putative Occ complex is currently limited by the scarcity of genetically tractable Betaproteobacteria.

Figure 2.
Figure 2. Gene arrangement, predicted protein location, and taxonomic distribution of major expressed respiratory complexes in “Ca. D. occultata”.

A: MtoDAB(Y)X porin-cytochrome c electron conduit; B: OccA-S; C: denitrification complexes (Nap, Nir, Nor and cNos); D: Occurrence of key marker genes in Betaproteobacteria and Gammaproteobacteria with >95% complete genomes that encode OccP. Protein sequences from “Ca. D. occultata” were used as query against a genome database and searched using PSI BLAST. Matches with identities >40%, query coverage >80% and E values <10−5 were considered positive. Red fill around genes and proteins indicate cytochrome-c proteins. Black outlines around blue circles in D indicate type I nitrous oxide reductase to distinguish from blue dots (type II/cytochrome-nitrous oxide reductase). Gray-shaded genes on the occ gene cluster indicate 6-NHL repeat proteins. Protein locations shown are based on P-sort predictions. Numbers above genes indicate number of CxxCH motifs predicted to bind cytochrome c. IM: inner membrane; OM: outer membrane. For more details, see Table 1 and Table S3.

View this table:
Table 1. Expression levels for “Ca. D. occultata” proteins in the presence of CH4 and N2.

Peptide identifications from mass spectrometry using Comet (Eng et al., 2013) were matched with a metagenome-generated protein database using Prokka (Seemann, 2014), or RAST for bins (Wattam et al., 2013; Overbeek et al., 2014). Database searches were completed on PeptideProphet (Nesvizhskii et al., 2003). Calculated false discovery rates (FDR) were <0.01. Normalized spectral abundances were calculated in QPROT with Abacus (Choi et al., 2015). Peptide counts are normalized to total “Ca. D. occultata” proteins x 10,000. Blank cells indicate proteins with <2 normalized peptide counts. Gray boxes indicate membrane proteins that may be underrepresented by mass spectrometry-based metaproteomic analyses, which inherently favor soluble over insoluble membrane-bound or hydrophobic proteins. SP: signal peptide (Y:present/N:absent); TMH: numbers of transmembrane helices; # CxxCH: number of heme-binding motifs; P-sort: predicted cellular location based on Psortb v.3.0. Bold proteins indicate proteins that were significantly more expressed with CH4 than N2 (CH4/N2>1; p<0.05). MCP: methyl-accepting chemotaxis protein; PPIase: Peptidyl-proline isomerase; P: periplasm, C: cytoplasm; OM: outer membrane; IM: inner membrane, E: extracellular; U: unknown. MtoX and MtoY were predicted to be an inner membrane cytochrome-b protein and a methyl-accepting chemotaxis protein, respectively.

Proteins with 40-60% identity to the expressed “Ca. D. occultata” OccP protein were widely distributed in Betaproteobacteria from diverse freshwaters and deep subsurface groundwaters, as well as several Gammaproteobacteria and one alphaproteobacterium (Fig. 2D; Table S3). Most occP-containing bacteria also possessed mtoA and denitrification genes (Fig. 2D; Figs. S7, S8). These results widen the phylogenetic and structural diversity of candidate extracellular MHCs that may be involved in microbial Mn(III) reduction.

Heme-copper oxidases in “Ca. D. occultata”

“Ca. D. occultata” expressed high-affinity cbb3-type cytochrome c oxidase (CcoNOQP) associated with microaerobic respiration (Table S4). Features of the “Ca. D. occultata”occS gene product, including conserved histidine residues (H-94, H-411, and H-413) that bind hemes a and a3, as well as the H-276 residue that binds CuB (Fig. S6), suggest that OccS may function similarly to CcoN, the terminal heme-copper oxidase proton pump in aerobic respiration. All identified OccS amino acid sequences lack CuB ligands Y-280 and H-403, and most lack CuB ligands H-325 and H-326. OccS sequences also lack polar and ionizable amino acids that comprise the well-studied D and K channels involved in proton translocation in characterized cytochrome c oxidases (Blomberg and Siegbahn, 2014), but contain conserved H, C, E, D, and Y residues that may serve as alternate proton translocation pathways, similar to those recently discovered in qNOR (Gonska et al., 2018). OccS homologs were also found in Azoarcus spp. and deep subsurface Betaproteobacteria (Fig. S6).

Expression of denitrification proteins and possible sources of oxidized nitrogen species

Periplasmic nitrate reductase (NapA), cytochrome nitrite reductase (NirS), and type II atypical nitrous oxide reductase (cNosZ; Fig. S7) were highly expressed by “Ca. D. occultata” (Table 1). Expression of the denitrification pathway was not expected because oxidized nitrogen species were not added to the medium, to which the only nitrogen supplied was NH4Cl (0.2 mM) and N2 in the headspace. Nitrification genes were not found in the metagenome. Because solid-phase Mn(III) is known to chemically oxidize NH4+ (Aigle et al., 2017; Boumaiza et al., 2018), we tested for abiotic NH4+ oxidation by soluble Mn(III) (1 mM). Ammonium concentrations remained unchanged, and no N2O or NOx- production was observed (Fig. S8), likely because our experiments lacked solid surfaces to mediate electron transfer. These findings are consistent with lack of detectable ammonium oxidation by Mn(III) pyrophosphate in estuarine sediments (Crowe et al., 2012). The close redox potential of Mn3+-pyrophosphate (~0.8 V; Yamaguchi and Sawyer, 1985)) to oxidized nitrogen species (0.35-0.75 V at circumneutral pH) and the lack of oxygen in the media could have induced the expression of denitrification genes simultaneously with Mn(III)-reduction genes. Gammaproteobacteria, for example, reduce Mn(III) even in the presence of nitrate (Kostka et al., 1995).

Carbon metabolism

“Ca. D. occultata” appeared to be growing mixotrophically. It expressed two CO2-assimilation pathways, a modified Calvin-Benson-Bassham (CBB) pathway, an open 3-hydroxypropionate (3-HP) pathway, the oxidative TCA cycle (including citrate synthase and 2-oxoglutarate dehydrogenase), and organic carbon transporters (Table S4; Fig. S9). Like D. agitata and D. denitrificans, the CBB pathway of “Ca. D. occultata” did not encode RuBisCO and sedoheptulose-1,7-bisphosphatase (SHbisPase; Fig. S10); SHbisPase may be replaced by 6-phosphofructokinase and an energy-generating pyrophosphatase (RIX41248; Kleiner et al., 2012; Zorz et al., 2018). A hypothetical signal peptide-containing protein (RIX43053) in between fructose-bisphosphatase and transkelotase was more highly expressed during growth on CH4 vs. N2. “Ca. D. occultata” also encodes citrate lyase and 2-oxoglutarate/ferredoxin oxidoreductase indicative of a reductive TCA cycle, but these enzymes were not detected in the proteomic data.

Methane stimulated Mn(III) reduction and cytochrome expression in “Ca. D. occultata” enrichment cultures. However, we did not detect isotopically labeled CO2 (Fig. S2) and proteomic evidence of carbon assimilation indicated that “Ca. D. occultata” assimilated organic carbon and not one-carbon compounds. “Ca. D. occultata” also expressed a PQQ-dependent methanol/ethanol dehydrogenase at higher levels in the presence of CH4 than N2 (p=0.03; Table 1). A PQQ-methanol dehydrogenase has been implicated in methylotrophy in Rhodocyclales (Kalyuzhnaya et al., 2008). Our search for any other genes that could encode proteins capable of CH4 oxidation recovered a cytochrome P450 (RIX47519) with 42% identity to Methylobacterium organophilum, which is capable of methanotrophy by an unknown mechanism (Green and Bousfield, 1983; Dedysh et al., 2004; Van Aken et al., 2004). Oxidation of methane to methanol by cytochrome P450 or another enzyme would serve as a substrate for pyrroloquinoline quinone (PQQ)-methanol dehydrogenase. However, RIX47519 was undetected in the proteomic data.

While the specific role of CH4 in Mn(III) reduction remains unknown, CH4 appeared to significantly stimulate expression of many cytochrome c proteins, including OccABGJK, MtoD-2, and cytochrome-c4 and -c5 proteins associated with anaerobic respiration (p < 0.05; Table 1; Fig. 2C). Expression of several “Ca. D. occultata” proteins involved in outer membrane structure and composition, including an extracellular DUF4214 protein located next to an S-layer protein similar to those involved in manganese binding and deposition (Wang et al., 2009), a serine protease possibly involved in Fe(III) particle attachment (Burns et al., 2009), an extracellular PEP-CTERM sorting protein for protein export (Haft et al., 2006), and a Tol-Pal system for outer membrane integrity, were also higher in the presence of CH4 (Table 1). Lack of proteomic and isotopic evidence for use of CH4 as an electron donor suggests that CH4 may be indirectly involved in Mn(III) reduction in “Ca. D. occultata”, possibly by lowering the redox potential of the cultures to favor higher rates of Mn(III) reduction than in N2-only cultures.

Transporters and sensors

Numerous transporters were present in the “Ca. D. occultata” genome, including 26 TonB-dependent siderophore transporters, 13 TRAP transporters for dicarboxylate transport, as well as ABC transporters for branched-chained amino acids and dipeptides and polypeptides (Table S4). “Ca. D. occultata” also contained a large number of environmental sensing genes: 52 bacterial hemoglobins with PAS-PAC sensors, 8 TonB-dependent receptors, and 8 NO responsive regulators (Dnr: Crp/fr family; Table S4). Uniquely in “Ca. D. occultata”, PAC-PAS sensors flanked accessory genes nosFLY on the c-nosZ operon (Fig. S7). Comparison of these flanking PAC-PAS sensors in “Ca. D. occultata” with O2-binding sensors revealed that an arginine ~20 aa upstream from the conserved histidine as the distal pocket ligand for O2-binding is not present in either sensor (Fig. S11), suggesting that the sensor may bind a different ligand, possibly NO, consistent with the placement of these genes next to cNosZ (Shimizu et al., 2015).

Nutrient storage

Active synthesis of storage polymers suggested that “Ca. D. occultata” was experiencing electron acceptor starvation at the time of harvesting, consistent with Mn(III) depletion in the bottles (Liu et al., 2015; Guanghuan et al., 2018). Polyphosphate-related proteins, including phosphate transporters, polyphosphate kinase, polyphosphatase, and poly-3-hydroxybutyrate synthesis machinery were detected in the proteome (Table S4). Polyphosphate-accumulating organisms store polyphosphates with energy generated from organic carbon oxidation during aerobic respiration or denitrification, which are later hydrolyzed when respiratory electron acceptors for ATP production are limiting. Cyanophycin was being actively synthesized for nitrogen storage.

Geobacter

“Ca. G. occultata ” expressed genes involved in the TCA cycle and subsequent pathways for energy-generation included citrate synthase, malate dehydrogenase, isocitrate dehydrogenase, fumarate hydratase and NADH-ubiquinone oxidoreductase at moderate abundance. “Ca. Geobacter occultata ” contained 17 multiheme c-type cytochromes, none of which were detected in the proteome. The lack of expression of electron transport and metal-reducing pathways makes it unlikely that “Ca. Geobacter occultata” was solely responsible for Mn(III) reduction observed in the incubations. It is possible that “Ca. G. occultata” and “Ca. D. occultata” engage in direct interspecies electron transport via e-pilins. A type IV pilin with 87% identity to Geobacter pickeringii (Holmes et al., 2016) was significantly more highly expressed with CH4 vs. N2 in the “Ca. G. occultata” proteome (p=0.02; Table 1). The possible involvement of Geobacter e-pilins in Mn(III) reduction remains an open question, due to the lack of studies examining the possibility of Mn(III) reduction in Deltaproteobacteria.

Conclusions

To our knowledge, this study provides the first evidence for biological reduction of soluble Mn(III) by a bacterium outside of the Gammaproteobacteria class. The dominant bacterium in Mn(III)-reducing enrichment cultures was “Ca. D. occultata”, a member of the Rhodocyclales order of Betaproteobacteria. “Ca. D. occultata” expressed decahemes similar to the Mto pathway, and occ genes, including a novel extracellular undecaheme (OccP), which are predicted to encode a new respiratory electron transport pathway. The novel occ operon was found to be widespread in Betaproteobacteria from the deep subsurface, where metal cycling can fuel microbial metabolism.

Puzzles remain about whether “Ca. D. occultata” can transform two potent greenhouse gases: methane and nitrous oxide. Although “Ca. D. occultata” was enriched with methane as the sole electron donor and cultures reduced Mn(III) more rapidly in the presence of CH4, no CH4 oxidation activity was measured in Mn(III)-reducing cultures, and proteomic data suggested that “Ca. D. occultata” was growing mixotrophically rather than assimilating CH4. It is possible than CH4 played an indirect role in Mn(III) reduction, perhaps by lowering the redox state of the cultures to conditions that were more favorable for anaerobic Mn(III) respiration. Further, although we did not add oxidized nitrogen compounds to our media, and Mn(III) did not chemically oxidize NH4+ under our culture conditions, type II nitrous oxide reductase (cNosZ) was one of the most abundant proteins expressed in Mn(III)-reducing cultures. The role of cNosZ and other denitrification enzymes in “Ca. D. occultata” metabolism, and their possible connection to Mn(III) reduction, remain to be investigated.

Competing Interests

The authors declare no competing interests.

Acknowledgements

This research was funded by NASA Exobiology grant NNX14AJ87G. Support was also provided by a Center for Dark Energy Biosphere Investigations (NSF-CDEBI OCE-0939564) small research grant and supported by the NASA Astrobiology Institute (NNA15BB03A) and a NASA Astrobiology Postdoctoral Fellowship to NS. SAC was supported through NSERC CRC, CFI, and Discovery grants. We thank Marcus Bray, Andrew Burns, Caleb Easterly, Pratik Jagtap, Cory Padilla, Angela Peña, Johnny Striepen, and Rowan Wolschleger for technical assistance. We thank Emily Weinert for helpful discussions.

Footnotes

  • Changed title to broaden implications. Combined main text and supplemental text. Clarified that protein expression changes in bottles with methane could be due to lower redox potential.

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Posted November 01, 2019.
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Novel insights into the taxonomic diversity and molecular mechanisms of bacterial Mn(III) reduction
Nadia Szeinbaum, Brook L. Nunn, Amanda R. Cavazos, Sean A. Crowe, Frank J. Stewart, Thomas J. DiChristina, Christopher T. Reinhard, Jennifer B. Glass
bioRxiv 695007; doi: https://doi.org/10.1101/695007
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