Hydrocarbon and Lipid Microbiology Protocols: Genetic, Genomic and System Analyses of Communities
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Unfortunately, concatenated ribosomal proteins are not able to provide clarity, which leaves some of the Acidobacteria MAGs from this study in undetermined subdivisions. Only Acidobacteria with confirmed subdivisions were analyzed for unique potential functions. This MAG has the functional potential to metabolize many carbon substrates including aromatic compounds, starch, glycogen, cellobiose, glucose, fructose, sucrose, maltose, and trehalose. Furthermore, this Amazon Acidobacterium has genes involved in nitrogen and sulfur cycling with the potential to reduce nitrite, nitric-oxide, sulfate, and sulfite.
Some features of interest were a nitric-oxide reductase quinol-dependent and a ubiquinol-cytochrome c reductase only found in Candidatus Obscuribacter phosphatis and the Amazon Melainabacteria.
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Similar to O. However, only the Amazon Melainabacteria MAG contains genes to synthesize cellulose from UDP-alpha- D -glucose and can potentially metabolize cellobiose, maltose, and xylose. This Amazon Melainabacteria MAG also contains genes for both aerobic and anaerobic respiration including a complete respiratory chain like O.
Among the features unique to Amazon-R is a complete particulate methane monooxygenase pmmo necessary for methane oxidation to methanol. A phylogenetic analysis of the pmmo alpha subunit pmoA found the Amazon-R pmoA to be unique and most closely related to pmoA genes from Streptomyces thermoautotrophicus , Nocardioides luteus , and Smaragdicoccus niigatensis Figure 4. The lateral gene transfer LGT analysis found that LGT-predicted genes are spread across many contigs supporting proper binning and none of the annotated genes were related to methane cycling Supplementary Table S8.
Phylogenetic tree of the particulate methane monooxygenase alpha subunit pmoA. The numbers on each node represent the bootstrap support. The majority of soil Rokubacteria MAGs 17 out of 22 have P enzymes necessary for the oxidation of large hydrocarbons. Rokubacteria MAGs 16 out of 53 contain genes for alkane 1-monooxygenase enzymes to oxidize shorter hydrocarbons.
Following hydrocarbon metabolism, Rokubacteria MAGs have the potential for beta-oxidation of fatty acids.
Enabled by the expanded dataset of 53 Rokubacteria MAGs, a conceptual metabolic model was formed based on annotated genes Figure 5 and Supplementary Table S This model is based on gene annotations without gap-filling and extends our knowledge of phylum Candidatus Rokubacteria. Rokubacteria MAGs have many metabolic capabilities including hydrocarbon metabolism, but the hydrocarbon methane can follow a different fate.
Methane can be oxidized through three enzymatic steps to formate, which can then follow several paths: 1 it can be converted to acetyl-CoA using the tetrahydrofolate H4F pathway, 2 it can be oxidized to carbon dioxide via formate dehydrogenase, or 3 it can be oxidized to carbon dioxide and hydrogen using a formate hydrogen lyase Figure 5.
Rokubacteria MAGs have the genomic potential to produce acetate and ethanol via the Wood—Ljungdahl pathway. There are genes for an electron transport Rnf complex in 20 Rokubacteria MAGs that is involved in energy generation. This phylum has the genomic potential to use all three central metabolic pathways and although there are signs of aerobic respiration, such as cytochrome c oxidase, there are also indications of anaerobic respiration including the potential to denitrify nitrate to nitrous oxide Supplementary Table S9.
Another possible electron acceptor is sulfate using dissimilatory sulfate reduction; although, there are also a few MAGs with assimilatory sulfate reduction genes Supplementary Table S9. The wide variety of carbon substrates, energy sources, and electron acceptors may help this phylum survive in varying environmental conditions.
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Indicated are the major metabolic processes including central carbon metabolism and energy generation in the center of the cell. The cell wall includes the various transporters, secretion systems, and electron transport complexes labeled by number. The legend for the cell wall box numbers is found in Supplementary Table S Our database contains six MAGs from the CPR superphylum Microgenomates, which correspond to the first soil genomic representatives of this large branch of the tree of life.
Phylogenetic analyses uncovered that the three genomes Amazon-Levybacteria, Amazon-Levybacteria, and Amazon-Levybacteria are most closely related to each other, and fall within Candidatus Levybacteria. MAGs Amazon-Pacebacteria, Amazon-Pacebacteria, and Amazon-Microgenomates are most closely related to each other with Amazon-Pacebacteria and Amazon-Pacebacteria forming a basal monophyletic clade with Candidatus Pacebacteria.
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Amazon-Microgenomates likely represents a novel candidate phylum within the superphylum Microgenomates based on its low mean amino acid identity compared to known phyla and its phylogenetic placement between Pacebacteria and Chisholmbacteria. Genes involved in DNA replication initiation DnaA , DnaB are still present, which supports that these organisms can possibly still replicate independently from a host.
An additional three genomes reconstructed from Amazon soil are most closely related to Candidatus Pacebacteria, one of which is thought to represent a novel phylum for which we propose the name Candidatus Cerribacteria. This phylum completely lacks the TCA cycle and is unable to produce acetyl-CoA or oxaloacetate to feed into the cycle. All genomes contain genes to use the one carbon pool by folate pathway, but none of them contain genes to perform folate biosynthesis except Amazon-Pacebacteria Additionally, Amazon-Pacebacteria encoded a cellulase protein necessary for cellulose metabolism.
Most of the unique genes from these MAGs encode hypothetical proteins. Amazon Parcubacteria have reduced metabolic capabilities, but potentially can break down various simple sugars to pyruvate using glycolysis and the pentose phosphate shunt, which is then converted to D -lactate. Amazon-Parcubacteria is also capable of synthesizing trehalose from glucosephosphate. Overall, the functional potential of soil Parcubacteria MAGs are in accordance with other studies, but Amazon Parcubacteria are phylogenetically distinct Supplementary Figure S6.
In this study, we investigated the impact of deforestation on the genomic diversity and functional potential of soil microorganisms using metagenomics and MAGs. Previous studies have examined how forest-to-pasture conversion in the Brazilian Amazon affects soil microbial communities Jesus et al.
Jesus et al. Our study concurs with Jesus et al. Previous work by Meyer et al.
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This study expands on work from Meyer et al. Furthermore, the two fast growing grass species grown in the pastures have been reported to secrete high quantities of labile C Reis et al. Lignin is a highly aromatic, recalcitrant carbon compound produced by plants Novaes et al. Previous work by Lammel et al. Using metagenomics, we found a differential abundance of genes related to lignin degradation in the rainforest and an increase in genes related to hemicellulose and cellulose degradation in the pasture soil. As the carbon sources available in each land-use type change, we see significant alterations to the microbial community composition with a higher abundance of Firmicutes in the pasture.
This is not unexpected since previous research has found that Firmicutes respond to increased organic matter Cleveland et al. We also observed an almost complete loss of the ammonia-oxidizing archaea Thaumarchaeota in the pasture soil, confirming earlier studies Hamaoui et al. A study by Subbarao et al. These Urochloa grasses that produce BNIs have been shown to inhibit both ammonia-oxidizing bacteria and archaea Moreta et al. By assembling MAGs, we have gained a new depth of insight into the putative life strategies of some Amazonian soil microorganisms that is not possible with only metagenomics.
In pastures we see a change in carbon metabolism coherent with results from our metagenomic data. These observed increases in fermentation and diversified carbon sources may have long-term consequences on carbon storage and greenhouse gas emissions. The abundance of Acidobacteria subdivisions have been previously found to significantly change between land-use types Navarrete et al. This group of non-photosynthetic fermenters have been found to metabolize cellulose and cellobiose in soil using stable isotope probing experiments Soo et al.
Both Amazon Acidobacteria subdivision 3 and Melainabacteria were found only in the pasture soil metagenomes likely playing an important role in metabolizing polycyclic aromatic hydrocarbons and plant-derived carbon deposited from the slash and burn deforestation practice. While we do not have the MAG replication to definitely test whether Acidobacteria subdivisions 3 and 4 and Melainabacteria are changing in abundance, we only detect their presence in one of the land uses, suggesting they are affected by land use change. Since Acidobacteria are considered ubiquitous in soils it is important to understand how the different subdivisions may be affected by land-use change.
All Microgenomates and Parcubacteria MAGs were found only in the pasture, suggesting these groups are also influenced by land use change.
Although the potential physiology of these candidate phyla MAGs was similar to what has previously been described Wrighton et al. With genomes examined, there is strong evidence that selection has or is occurring either for the loss of DNA mismatch repair in subsurface Microgenomates or for our Amazon soil Microgenomates to retain such machinery.
These mismatch repair proteins provide DNA stability under the stress of environmental fluctuations, which in the case of cattle pasture may be temperature, moisture, and UV radiation Denamur et al. In pathogenic or endosymbiotic bacteria, the loss of DNA repair and recombination proteins increases mutation rates which is thought to cause AT bias in small genomes Moran and Wernegreen, In rainforest soil we found a differential abundance of genes related to methanotrophy as has been previously reported by Meyer et al.
Rokubacteria have been described to oxidize methanol Butterfield et al. This discovery led to an investigation into potential hydrocarbon metabolism that appears to be wide-spread in the soil MAGs. An electron transport Rnf complex was found in many of the Rokubacteria MAGs, which is suggested to be essential for ATP synthesis in some acetogens when grown autotrophically on H 2 and CO 2 by creating a proton motive force Biegel et al.
Our expanded analyses of the Rokubacteria MAGs indicate a diverse metabolism within this phylum including a wide variety of carbon sources ranging from gaseous substrates to complex hydrocarbons, many possible energy sources, and electron acceptors. The combination of metagenome and MAG analyses allowed for increased understanding of the potential biological functions altered by land-use change.
Carbon cycling in both datasets appeared to be significantly altered by deforestation, especially related to complex carbon sources like lignin and polycyclic aromatic hydrocarbons. This study provides the basis for continuing research into how deforestation affects soil microbial communities, biogeochemical cycling, and for the first-time tropical soil candidate phyla. MK contributed all metagenome and MAG analyses, all statistical analyses, drafted the manuscript, and drafted the figures and tables.
JG contributed metagenome co-assembly and critical review of manuscript. ST and KK contributed in revising of manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank the owners and staff of Agropecuaria Nova Vida for logistical support and permission to work on their property. Alneberg, J. Binning metagenomic contigs by coverage and composition.
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Biegel, E. Biochemistry evolution and physiological function of the Rnf complex a novel ion-motive electron transport complex in prokaryotes. Life Sci. Borneman, J. Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. PubMed Abstract Google Scholar. Bowers, R. Brown, C.