Priorities, opportunities, and challenges for integrating microorganisms into Earth system models for climate change prediction.

Climate change jeopardizes human health, global biodiversity, and sustainability of the biosphere. To make reliable predictions about climate change, scientists use Earth system models (ESMs) that integrate physical, chemical, and biological processes occurring on land, the oceans, and the atmosphere. Although critical for catalyzing coupled biogeochemical processes, microorganisms have traditionally been left out of ESMs. Here, we generate a "top 10" list of priorities, opportunities, and challenges for the explicit integration of microorganisms into ESMs. We discuss the need for coarse-graining microbial information into functionally relevant categories, as well as the capacity for microorganisms to rapidly evolve in response to climate-change drivers. Microbiologists are uniquely positioned to collect novel and valuable information necessary for next-generation ESMs, but this requires data harmonization and transdisciplinary collaboration to effectively guide adaptation strategies and mitigation policy.

Evolution of a minimal cell.

Possessing only essential genes, a minimal cell can reveal mechanisms and processes that are critical for the persistence and stability of life1,2. Here we report on how an engineered minimal cell3,4 contends with the forces of evolution compared with the Mycoplasma mycoides non-minimal cell from which it was synthetically derived. Mutation rates were the highest among all reported bacteria, but were not affected by genome minimization. Genome streamlining was costly, leading to a decrease in fitness of greater than 50%, but this deficit was regained during 2,000 generations of evolution. Despite selection acting on distinct genetic targets, increases in the maximum growth rate of the synthetic cells were comparable. Moreover, when performance was assessed by relative fitness, the minimal cell evolved 39% faster than the non-minimal cell. The only apparent constraint involved the evolution of cell size. The size of the non-minimal cell increased by 80%, whereas the minimal cell remained the same. This pattern reflected epistatic effects of mutations in ftsZ, which encodes a tubulin-homologue protein that regulates cell division and morphology5,6. Our findings demonstrate that natural selection can rapidly increase the fitness of one of the simplest autonomously growing organisms. Understanding how species with small genomes overcome evolutionary challenges provides critical insights into the persistence of host-associated endosymbionts, the stability of streamlined chassis for biotechnology and the targeted refinement of synthetically engineered cells2,7-9.

Microbiology and Climate Change: a Transdisciplinary Imperative.

Climate change is a complex problem involving nonlinearities and feedback that operate across scales. No single discipline or way of thinking can effectively address the climate crisis. Teams of natural scientists, social scientists, engineers, economists, and policymakers must work together to understand, predict, and mitigate the rapidly accelerating impacts of climate change. Transdisciplinary approaches are urgently needed to address the role that microorganisms play in climate change. Here, we demonstrate with case studies how diverse teams and perspectives provide climate-change insight related to the range expansion of emerging fungal pathogens, technological solutions for harmful cyanobacterial blooms, and the prediction of disease-causing microorganisms and their vector populations using massive networks of monitoring stations. To serve as valuable members of a transdisciplinary climate research team, microbiologists must reach beyond the boundaries of their immediate areas of scientific expertise and engage in efforts to build open-minded teams aimed at scalable technologies and adoptable policies.

Phage-Encoded Sigma Factors Alter Bacterial Dormancy.

By entering a reversible state of reduced metabolic activity, dormant microorganisms are able to tolerate suboptimal conditions that would otherwise reduce their fitness. Dormancy may also benefit bacteria by serving as a refuge from parasitic infections. Here, we focus on dormancy in the Bacillota, where endospore development is transcriptionally regulated by the expression of sigma factors. A disruption of this process could influence the survivorship or reproduction of phages that infect spore-forming hosts with implications for coevolutionary dynamics. We characterized the distribution of sigma factors in over 4,000 genomes of diverse phages capable of infecting hosts that span the bacterial domain. From this, we identified homologs of sporulation-specific sigma factors in phages that infect spore-forming hosts. Unlike sigma factors required for phage reproduction, we provide evidence that sporulation-like sigma factors are nonessential for lytic infection. However, when expressed in the spore-forming Bacillus subtilis, some of these phage-derived sigma factors can activate the bacterial sporulation gene network and lead to a reduction in spore yield. Our findings suggest that the acquisition of host-like transcriptional regulators may allow phages to manipulate a complex and ancient trait in one of the most abundant cell types on Earth. IMPORTANCE As obligate parasites, phages exert strong top-down pressure on host populations with eco-evolutionary implications for community dynamics and ecosystem functioning. The process of phage infection, however, is constrained by bottom-up processes that influence the energetic and nutritional status of susceptible hosts. Many phages have acquired auxiliary genes from bacteria, which can be used to exploit host metabolism with consequences for phage fitness. In this study, we demonstrate that phages infecting spore-forming bacteria carry homologs of sigma factors, which their hosts use to orchestrate gene expression during spore development. By tapping into regulatory gene networks, phages may manipulate the physiology and survival strategies of nongrowing bacteria in ways that influence host-parasite coevolution.

Dormancy dampens the microbial distance-decay relationship.

Much of Earth's biodiversity has the capacity to engage in dormancy, a reversible state of reduced metabolic activity. By increasing resilience to unfavourable conditions, dormancy leads to the accumulation of 'seed banks'. These reservoirs of genetic and phenotypic diversity should diminish the strength of environmental filtering and increase rates of dispersal. Although prevalent among single-celled organisms, evidence that dormancy influences patterns of microbial biogeography is lacking. We constructed geographical and environmental distance-decay relationships (DDRs) for the total (DNA) and active (RNA) portions of bacterial communities in a regional-scale 16S rRNA survey of forested ponds in Indiana, USA. As predicted, total communities harboured greater diversity and exhibited weaker DDRs than active communities. These observations were robust to random resampling and different community metrics. To evaluate the processes underlying the biogeographic patterns, we developed a platform of mechanistic models that used the geographical coordinates and environmental characteristics of our study system. Based on more than 106 simulations, our models approximated the empirical DDRs when there was strong environmental filtering along with the presence of long-lived seed banks. By contrast, the inclusion of dispersal generally decreased model performance. Together, our findings support recent theoretical predictions that seed banks can influence the biogeographic patterns of microbial communities. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

How, When, and Where Relic DNA Affects Microbial Diversity.

Extracellular or "relic" DNA is one of the largest pools of nucleic acids in the biosphere. Relic DNA can influence a number of important ecological and evolutionary processes, but it may also affect estimates of microbial abundance and diversity, which has implications for understanding environmental, engineered, and host-associated ecosystems. We developed models capturing the fundamental processes that regulate the size and composition of the relic DNA pools to identify scenarios leading to biased estimates of biodiversity. Our models predict that bias increases with relic DNA pool size, but only when the species abundance distributions (SADs) of relic and intact DNA are distinct from one another. We evaluated our model predictions by quantifying relic DNA and assessing its contribution to bacterial diversity using 16S rRNA gene sequences collected from different ecosystem types, including soil, sediment, water, and the mammalian gut. On average, relic DNA made up 33% of the total bacterial DNA pool but exceeded 80% in some samples. Despite its abundance, relic DNA had a minimal effect on estimates of taxonomic and phylogenetic diversity, even in ecosystems where processes such as the physical protection of relic DNA are common and predicted by our models to generate bias. Our findings are consistent with the expectation that relic DNA from different taxa degrades at a constant and equal rate, suggesting that it may not fundamentally alter estimates of microbial diversity.IMPORTANCE The ability to rapidly obtain millions of gene sequences and transcripts from a range of environments has greatly advanced understanding of the processes that regulate microbial communities. However, nucleic acids extracted from complex samples do not come only from viable microorganisms. Dead microorganisms can generate large pools of relic DNA that distort insight into the ecology and evolution of microbial systems. Here, we develop a conceptual and quantitative framework for understanding how relic DNA influences the structure of microbiomes. Our theoretical models and empirical results demonstrate that a large relic DNA pool does not automatically lead to biased estimates of microbial diversity. Rather, relic DNA effects emerge in combination with microscale processes that alter the commonness and rarity of sequences found in heterogeneous DNA pools.

Whole-Genome Sequence of the Soil Bacterium Micrococcus sp. KBS0714.

We present here a draft genome assembly of Micrococcus sp. KBS0714, which was isolated from agricultural soil. The genome provides insight into the strategies that Micrococcus spp. use to contend with environmental stressors such as desiccation and starvation in environmental and host-associated ecosystems.

Microbial contributions to subterranean methane sinks.

Sources and sinks of methane (CH4 ) are critical for understanding global biogeochemical cycles and their role in climate change. A growing number of studies have reported that CH4 concentrations in cave ecosystems are depleted, leading to the notion that these subterranean environments may act as sinks for atmospheric CH4 . Recently, it was hypothesized that this CH4 depletion may be caused by radiolysis, an abiotic process whereby CH4 is oxidized via interactions with ionizing radiation derived from radioactive decay. An alternate explanation is that the depletion of CH4 concentrations in caves could be due to biological processes, specifically oxidation by methanotrophic bacteria. We theoretically explored the radiolysis hypothesis and conclude that it is a kinetically constrained process that is unlikely to lead to the rapid loss of CH4 in subterranean environments. We present results from a controlled laboratory experiment to support this claim. We then tested the microbial oxidation hypothesis with a set of mesocosm experiments that were conducted in two Vietnamese caves. Our results reveal that methanotrophic bacteria associated with cave rocks consume CH4 at a rate of 1.3-2.7 mg CH4  · m-2  · d-1 . These CH4 oxidation rates equal or exceed what has been reported in other habitats, including agricultural systems, grasslands, deciduous forests, and Arctic tundra. Together, our results suggest that depleted concentrations of CH4 in caves are most likely due to microbial activity, not radiolysis as has been recently claimed. Microbial methanotrophy has the potential to oxidize CH4 not only in caves, but also in smaller-size open subterranean spaces, such as cracks, fissures, and other pores that are connected to and rapidly exchange with the atmosphere. Future studies are needed to understand how subterranean CH4 oxidation scales up to affect local, regional, and global CH4 cycling.

Microscale Insight into Microbial Seed Banks.

Microbial dormancy leads to the emergence of seed banks in environmental, engineered, and host-associated ecosystems. These seed banks act as reservoirs of diversity that allow microbes to persist under adverse conditions, including extreme limitation of resources. While microbial seed banks may be influenced by macroscale factors, such as the supply of resources, the importance of microscale encounters between organisms and resource particles is often overlooked. We hypothesized that dimensions of spatial, trophic, and resource complexity determine rates of encounter, which in turn, drive the abundance, productivity, and size of seed banks. We tested this using >10,000 stochastic individual based models (IBMs) that simulated energetic, physiological, and ecological processes across combinations of resource, spatial, and trophic complexity. These IBMs allowed realistic dynamics and the emergence of seed banks from ecological selection on random variation in species traits. Macroscale factors like the supply and concentration of resources had little effect on resource encounter rates. In contrast, encounter rates were strongly influenced by interactions between dispersal mode and spatial structure, and also by the recalcitrance of resources. In turn, encounter rates drove abundance, productivity, and seed bank dynamics. Time series revealed that energetically costly traits can lead to large seed banks and that recalcitrant resources can lead to greater stability through the formation of seed banks and the slow consumption of resources. Our findings suggest that microbial seed banks emerge from microscale dimensions of ecological complexity and their influence on resource limitation and energetic costs.