Deforestation in the Brazilian Amazon occurs at an alarming rate, which has broad effects on global greenhouse gas emissions, carbon storage, and biogeochemical cycles. In this study, soil metagenomes and metagenome-assembled genomes (MAGs) were analyzed for alterations to microbial community composition, functional groups, and putative physiology as it related to land-use change and tropical soil. A total of 28 MAGs were assembled encompassing 10 phyla, including both dominant and rare biosphere lineages. Amazon Acidobacteria subdivision 3, Melainabacteria, Microgenomates, and Parcubacteria were found exclusively in pasture soil samples, while Candidatus Rokubacteria was predominant in the adjacent rainforest soil. These shifts in relative abundance between land-use types were supported by the different putative physiologies and life strategies employed by the taxa. This research provides unique biological insights into candidate phyla in tropical soil and how deforestation may impact the carbon cycle and affect climate change.

Amazonian rainforest is undergoing increasing rates of deforestation, driven primarily by cattle pasture expansion. Forest-to-pasture conversion has been associated with increases in soil methane (CH₄) emission. To better understand the drivers of this change, we measured soil CH₄ flux, environmental conditions, and belowground microbial community structure across primary forests, cattle pastures, and secondary forests in two Amazonian regions. We show that pasture soils emit high levels of CH₄ (mean: 3454.6 ± 9482.3 μg CH₄ m^-2 d^-1), consistent with previous reports, while forest soils on average emit CH₄ at modest rates (mean: 9.8 ± 120.5 μg CH₄ m^-2 d^-1), but often act as CH₄ sinks. We report that secondary forest soils tend to consume CH₄ (mean: -10.2 ± 35.7 μg CH₄ m^-2 d^-1), demonstrating that pasture CH₄ emissions can be reversed. We apply a novel computational approach to identify microbial community attributes associated with flux independent of soil chemistry. While this revealed taxa known to produce or consume CH₄ directly (i.e. methanogens and methanotrophs, respectively), the vast majority of identified taxa are not known to cycle CH₄. Each land use type had a unique subset of taxa associated with CH₄ flux, suggesting that land use change alters CH₄ cycling through shifts in microbial community composition. Taken together, we show that microbial composition is crucial for understanding the observed CH₄ dynamics and that microorganisms provide explanatory power that cannot be captured by environmental variables.

The Amazon rainforest is a biodiversity hotspot and large terrestrial carbon sink threatened by agricultural conversion. Rainforest-to-pasture conversion stimulates the release of methane, a potent greenhouse gas. The biotic methane cycle is driven by microorganisms; therefore, this study focused on active methane-cycling microorganisms and their functions across land-use types. We collected intact soil cores from three land use types (primary rainforest, pasture, and secondary rainforest) of two geographically distinct areas of the Brazilian Amazon (Santarém, Pará and Ariquemes, Rondônia) and performed DNA stable-isotope probing coupled with metagenomics to identify the active methanotrophs and methanogens. At both locations, we observed a significant change in the composition of the isotope-labeled methane-cycling microbial community across land use types, specifically an increase in the abundance and diversity of active methanogens in pastures. We conclude that a significant increase in the abundance and activity of methanogens in pasture soils could drive increased soil methane emissions. Furthermore, we found that secondary rainforests had decreased methanogenic activity similar to primary rainforests, and thus a potential to recover as methane sinks, making it conceivable for forest restoration to offset greenhouse gas emissions in the tropics. These findings are critical for informing land management practices and global tropical rainforest conservation.