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ABSTRACT Below-ground carbon transformations that contribute to healthy soils represent a natural climate change mitigation, but newly acquired traits adaptive to climate stress may alter microbial feedback mechanisms. To better define microbial evolutionary responses to long-term climate warming, we study microorganisms from an ongoingin situsoil warming experiment where, for over three decades, temperate forest soils are continuously heated at 5°C above ambient. We hypothesize that across generations of chronic warming, genomic signatures within diverse bacterial lineages reflect adaptations related to growth and carbon utilization. From our bacterial culture collection isolated from experimental heated and control plots, we sequenced genomes representing dominant taxa sensitive to warming, including lineages of Actinobacteria, Alphaproteobacteria, and Betaproteobacteria. We investigated genomic attributes and functional gene content to identify signatures of adaptation. Comparative pangenomics revealed accessory gene clusters related to central metabolism, competition, and carbon substrate degradation, with few functional annotations explicitly associated with long-term warming. Trends in functional gene patterns suggest genomes from heated plots were relatively enriched in central carbohydrate and nitrogen metabolism pathways, while genomes from control plots were relatively enriched in amino acid and fatty acid metabolism pathways. We observed that genomes from heated plots had less codon bias, suggesting potential adaptive traits related to growth or growth efficiency. Codon usage bias varied for organisms with similar 16Srrnoperon copy number, suggesting that these organisms experience different selective pressures on growth efficiency. Our work suggests the emergence of lineage-specific trends as well as common ecological-evolutionary microbial responses to climate change.IMPORTANCEAnthropogenic climate change threatens soil ecosystem health in part by altering below-ground carbon cycling carried out by microbes. Microbial evolutionary responses are often overshadowed by community-level ecological responses, but adaptive responses represent potential changes in traits and functional potential that may alter ecosystem function. We predict that microbes are adapting to climate change stressors like soil warming. To test this, we analyzed the genomes of bacteria from a soil warming experiment where soil plots have been experimentally heated 5°C above ambient for over 30 years. While genomic attributes were unchanged by long-term warming, we observed trends in functional gene content related to carbon and nitrogen usage and genomic indicators of growth efficiency. These responses may represent new parameters in how soil ecosystems feedback to the climate system. 

ABSTRACT The evolution of oxygenic photosynthesis in the Cyanobacteria was one of the most transformative events in Earth history, eventually leading to the oxygenation of Earth’s atmosphere. However, it is difficult to understand how the earliest Cyanobacteria functioned or evolved on early Earth in part because we do not understand their ecology, including the environments in which they lived. Here, we use a cutting-edge bioinformatics tool to survey nearly 500,000 metagenomes for relatives of the taxa that likely bookended the evolution of oxygenic photosynthesis to identify the modern environments in which these organisms live. Ancestral state reconstruction suggests that the common ancestors of these organisms lived in terrestrial (soil and/or freshwater) environments. This restricted distribution may have increased the lag between the evolution of oxygenic photosynthesis and the oxygenation of Earth’s atmosphere.IMPORTANCECyanobacteria generate oxygen as part of their metabolism and are responsible for the rise of oxygen in Earth’s atmosphere over two billion years ago. However, we do not know how long this process may have taken. To help constrain how long this process would have taken, it is necessary to understand where the earliest Cyanobacteria may have lived. Here, we use a cutting-edge bioinformatics tool called branch water to examine the environments where modern Cyanobacteria and their relatives live to constrain those inhabited by the earliest Cyanobacteria. We find that these species likely lived in non-marine environments. This indicates that the rise of oxygen may have taken longer than previously believed. 

ABSTRACT Methanotrophic bacteria play a vital role in the biogeochemical carbon cycle due to their unique ability to use CH₄as a carbon and energy source. Evidence suggests that some methanotrophs, includingMethylococcus capsulatus, can also use CO₂as a carbon source, making these bacteria promising candidates for developing biotechnologies targeting greenhouse gas capture and mitigation. However, a deeper understanding of the dual CH₄and CO₂metabolism is needed to guide methanotroph strain improvements and realize their industrial utility. In this study, we show thatM. capsulatusexpresses five carbonic anhydrase (CA) isoforms, one α-CA, one γ-CA, and three β-CAs, that play a role in its inorganic carbon metabolism and CO₂-dependent growth. The CA isoforms are differentially expressed, and transcription of all isoform genes is induced in response to CO₂limitation. CA null mutant strains exhibited markedly impaired growth compared to an isogenic wild-type control, suggesting that the CA isoforms have independent, non-redundant roles inM. capsulatusmetabolism and physiology. Overexpression of some, but not all, CA isoforms improved bacterial growth kinetics and decreased CO₂evolution from CH₄-consuming cultures. Notably, we developed an engineered methanotrophic biocatalyst overexpressing the native α-CA and β-CA with a 2.5-fold improvement in the conversion of CH₄to biomass. Given that product yield is a significant cost driver of methanotroph-based bioprocesses, the engineered strain developed here could improve the economics of CH₄biocatalysis, including the production of single-cell protein from natural gas or anaerobic digestion-derived biogas.IMPORTANCEMethanotrophs transform CH₄into CO₂and multi-carbon compounds, so they play a critical role in the global carbon cycle and are of interest for biotechnology applications. Some methanotrophs, includingMethylococcus capsulatus, can also use CO₂as a carbon source, but this dual one-carbon metabolism is incompletely understood. In this study, we show thatM. capsulatuscarbonic anhydrases are critical for this bacterium to optimally utilize CO₂. We developed an engineered strain with improved CO₂utilization capacity that increased the overall carbon conversion to cell biomass. The improvements to methanotroph-based product yields observed here are expected to reduce costs associated with CH₄conversion bioprocesses. 

ABSTRACT Biological complexity is widely seen as the central, intractable challenge of engineering biology. Yet this challenge has been constructed through the field’s dominant metaphors. Alternative ways of thinking—latent in progressive experimental approaches, but rarely articulated as such—could instead position complexity as engineering biology’s greatest resource. We outline how assumptions about engineered microorganisms have been built into the field, carried by entrenched metaphors, even as contemporary methods move beyond them. We suggest that alternative metaphors would better align engineering biology’s conceptual infrastructure with the field’s move away from conventionally engineering-inspired methods toward biology-centric ones. Innovating new conceptual frameworks would also enable better aligning scientific work with higher-level conversations about that work. Such innovation—thinking about how engineering microbes might be more like user-centered design than like programming a computer or building a car—could highlight complexity as a resource to leverage, not a problem to erase or negate.