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Microbial Communities and Interactions of Nitrogen Oxides with Methanogenesis in Diverse Peatlands of the Amazon Basin

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Microbial Communities and Interactions of Nitrogen Oxides with Methanogenesis in Diverse Peatlands of the Amazon Basin Supplementary Material Microbial Communities and Interactions of Nitrogen Oxides With Methanogenesis in Diverse Peatlands of the Amazon Basin S. Buessecker, Z. Zamora, A. F. Sarno, D. R. Finn, A. M. Hoyt, J. van Haren, J. D. Urquiza Muñoz, and H. Cadillo-Quiroz Correspondence to: H. Cadillo-Quiroz ([email protected]) Supplementary Material 1 Supplementary Discussion Dissolved organic carbon (DOC) profiles. DOC has emerged as an important predictor of CH4 production in wetland soils (Liu et al., 2012; Morrissey et al., 2013). In comparison, DOC concentrations obtained in this study are at the lower end of values previously reported from Borneo peats (Gandois et al., 2014). All concentration profiles appear stable along soil depth with no indication of sinks. These would conceivably occur in more shallow regions where the fraction of refractory soil carbon is less prevalent (Artz et al., 2006). A DOC sink due to mineralization is not present based on our data. The DOC pool is comprised of diverse organic molecules characterized by a wide molecular size range, organic acids, humic substances of different aromaticities, and protein groups. These compounds may vary with depth even though the bulk concentration may be stagnant. Extracellular enzymes and humic substances may play a crucial role in diverting electron flow from methanogenesis, given the thermodynamic preference over CO2 (Heitmann et al., 2007; Knorr and Blodau, 2009), that would ultimately suppress CH4 production. Based on our results, we can exclude fluctuations of the total DOC pool to have major effects on carbon mineralization in distinct soil layers, but organic compounds could structurally differ along depth and impact specific microbial activities. Xanthobacteriaceae and Bathyarchaeota are potentially important decomposers of organic matter in tropical peat soils. The high abundance of Xanthobacteriaceae and Bathyarchaeota (Fig. S3) across sites is likely related to a putative role as degraders of peat organic matter. Particularly under O2-limiting conditions, Xanthobacteriaceae have a broad suite of organic substrates, including alkanes, alkenes, (poly)aromatic compounds, thiopenes, organic acids, or xylose and xylan (Zaichikova et al., 2010). Those substrates are common and accumulate in peat soils 2 (Moers et al., 1990). Bathyarchaeota is an abundant group likely to have been overlooked by the lack of recognition of the phyla in older databases (as in SILVA 115 or priors; (Bai et al., 2018), or because several primers are incapable of amplification (like the mcrA set in this study that has 10-18 base pair mismatches; (Evans et al., 2015)). The genetic potential of Bathyarchaeota includes enzymes to hydrolyze plant-derived carbohydrates and detrital proteins, and to produce acetate for energy conservation (Lazar et al., 2016). A putative relationship Bathyarchaeota-NOx is supported by – – a report indicating that NO2 /NO3 transporter proteins, an enzymatic set to support DNRA, were detected in reconstructed Bathyarchaeota metagenomes (Lazar et al., 2016). PC analysis indicates such interactions, where Bathyarchaeota diversity, pH and NOx concomitantly explain over 50% of data variation along PC 1 (Fig. 2B). 3 Supplementary Material 2 Supplementary Figures and Tables 2.1 Supplementary Figures Supplementary Figure 1. Left panel: Ca/Mg ratio in lines for QUI (dashed), BVA (solid), and SJO (point-dashed). pH in symbols for QUI (circles), SJO (triangles), and BVA (squares). Each point is 3– derived from one replicate soil core. Middle panel: PO4 concentration with data points 2– representing the mean of values from replicate soil cores. Right panel: SO4 concentration with data points representing the mean of values from replicate soil cores. Error bars denote one SD and symbols are consistent with left panel. Pore water of SJO strongly resembles rainwater composition (Ca/Mg mean of ~8.8, Honório et al., 2010). BVA is likely influenced by groundwater (vertical or lateral water movements) that provides the peat body with minerals. Minerotrophic peatlands have a mineral-derived alkalinity that counteracts acidification caused by the degradation of plant litter and the release of organic acids. Ombrotrophic peatlands are characterized by a low basic cation content that lacks buffer capacity. BVA is a minerotrophic site, where as QUI is transitional minerotrophic-ombrotrophic. SJO is strictly ombrotrophic and the convex shape of this peatland further induces a barrier for groundwater to reach top soil layers (Lähteenoja et al., 2009). 4 Supplementary Figure 2. Dissolved oxygen concentration in water of saturated soil. Measurements were done using a microelectrode, which was either inserted directly into soft peat (red symbols) or into a shallow (~3 cm) water pond (blue symbols). Measurements were conducted in QUI peatland showing O2 concentrations drop below 1 µM detection levels after 1 or 2.7 cm depths. 5 Supplementary Material QUI, 16S SJO, 16S BVA, 16S Supplementary Figure 3. Alpha-rarefaction curves for 16S rRNA sequences, used to adjust for variability in library size across samples. Rarefaction curves were used to determine the minimum number of reads per sample used for alpha diversity metrics. 6 QUI, mcrA SJO, mcrA BVA, mcrA Supplementary Figure 3 continued. Alpha-rarefaction curves for mcrA sequences, used to adjust for variability in library size across samples. Rarefaction curves were used to determine the minimum number of reads per sample used for alpha diversity metrics. Samples were rarefied to 20,000 reads per sample (Yang et al., 2017). 7 Supplementary Material 100 Methanosarcinaceae_clone 96 Methanosarcina_barkeri_(Y00158) 57 Methanosaetaceae_clone Methanocellaceae_clone 70 100 Rice_Cluster_I_clone Methanomicrobia 100 Rice_Cluster_II_clone Methanomicrobiaceae_clone Methanoregulaceae_clone 100 100 unclassified_Methanomicrobia_clone 89 Methanoregula_boonei_(CP000780) 16S rRNA Methanobacteriaceae_clone 100 Methanobacterium_lacus_(CP002551) Methanobacteria Marine_Benthic_Group_D_clone unclassified_Thermoplasmatales_clone 99 Thermoplasmata 99 Thermoplasmatales_Incertae_Sedis_clone 0.050 100 Methanoregulaceae_clone 94 Methanoregula_boonei_(CP000780) Methanocalculaceae_clone 84 94 Methanospirillum_clone Methanomicrobia 59 Methanosaetaceae_clone Candidatus_Methanoperedenaceae_clone 90 Methanosarcina_clone 100 Methanosarcina_barkeri_(Y00158) mcrA Methanobacterium_clone Methanobacteria 100 Methanobacterium_lacus_(CP002551) Methanomassiliicoccaceae_clone Thermoplasmata 99 Methanomicrobial_Arc_I_group_clone 0.10 Supplementary Figure 4. 16S rRNA and mcrA phylogenetic trees based on the neighbor-joining method and 100 iterations. The trees reflect congruency of classified sequences from 16S and mcrA amplicon sequencing. 8 pH-meter Soil slurry (pH, soil temperature) Microelectrode (dissolved O2) IC (Anions, cations) TOC analyzer (DOC) directmeasurement Spectrophotometer (inorganic nitrogen) Pore water PTFE/Teflon tubing IR-MS (DI13C) Field work GC (CH4, CO2, N2O) Gas PTFE/Teflon tubing IR-MS (13CH4) N2O-reducing methanogenic cultures sampling ICP-MS (Mo) mcrA and archaeal 16S rRNA Soil Soil corer gene quantities Molecular analyses pipeline whole community and methanogen diversity 97% identity Taxonomic Dereplication* clustering* classification PCR barcoding Chimera Singleton (VSEARCH)* Illumina Merging, filtering* filtering* genomic 16SrRNA *Qiime 2 DNA MiSeq demultiplexing Phylogenetic **Usearch standard Translation, Singleton extraction sequencing tree (Mega7) prep. Dereplication** frameshift correction filtering** (Framebot) Taxonomic Chimera 85% identity mcrA qPCR classification filtering** clustering** (BlastP) Laboratory computational analysis Supplementary Figure 5. Workflow overview including the molecular analysis pipeline. 9 Supplementary Material Biplot Biplot 4 A 4 B 3 Phophate Thaumarchaeota OTUs 2 Nitrospirae OTUs 2 1 pH Shannon [Nitrate] (mcrA) 0 0 [Nitrite] -1 Unifrac Component 2 (16.8 %) Component 2 (16.4 %) (mcrA) [Nitrite] -2 -2 [Nitrate] -3 -4 Principal-4 Components:onCorrelations PrincipalComponents:onCorrelations -4 -3 -2 -1 01234 -4 -2 0 24 Biplot Component 1 (56 %) Biplot Component 1 (61.4 %) 4 4 C D 3 3 Unifrac (Bathyarchaeota) [Methane] 2 2 1 1 Bathyarchaeota [Nitrate] OTUs 0 0 pH -1 -1 Methanobacteria [Nitrite] Component 2 (18.3 %) Component 2 (13.7 %) OTUs Shannon mcrA gene copies -2 -2 (Bathyarchaeota) Methanomicrobia OTUs -3 -3 Principal-4 Components:onCorrelations Principal-4 Components:onCorrelations -4 -3 -2 -1 01234 -4 -3 -2 -1 01234 Biplot Component 1 (66.8 %) Biplot Component 1 (52.9 %) 3 4 Shannon (Methanobacteria) E F 3 2 [Nitrite] Unifrac (Methanomicrobia) 2 pH 1 1 [Nitrate] [Nitrate] 0 0 -1 pH Component 2 (16.6 %) Component 2 (33.4 %) -1 [Nitrite] -2 Shannon Unifrac -2 (Methanomicrobia) (Methanobacteria) -3 -3 -4 -3 -2 -1 0123 -4 -3 -2 -1 01234 Component 1 (45.5 %) Component 1 (52.2 %) Supplementary Figure 6. Principal component Analysis (PCA) ordination plots of microbial and environmental data from three soil profiles of contrasting Amazon peatlands. Samples were derived from QUI (triangles), SJO (circles) and BVA (squares) with abbreviations as in Fig. 1. Extended environmental variables or microbial groups were evaluated against overall microbial communities variation. Figure 3 in main text is identical to panels C and D. 10 36 Methanofollis liminatans (Q977G7) 62 Methanoregula formicica (A0A0H4CQL0) Methanomicrobium mobile (Q977G4) 56 79 Methanoplanus limicola (F4N9N6) 53 Methanosphaerula palustris (A9YUI5) OTU 22
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