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ABSTRACT Microorganisms play a central role in sustaining soil ecosystems and agriculture, and these functions are usually associated with their complex life history. Yet, the regulation and evolution of life history have remained enigmatic and poorly understood, especially in protozoa, the third most abundant group of organisms in the soil. Here, we explore the life history of a cosmopolitan species—Colpoda steinii. Our analysis has yielded a high-quality macronuclear genome forC. steinii, with size of 155 Mbp and 37,123 protein-coding genes, as well as mean intron length of ~93 bp, longer than most other studied ciliates. Notably, we identify two possible whole-genome duplication events inC. steinii, which may account for its genome being about twice the size ofC. inflata’s, another co-existing species. We further resolve the gene expression profiles in diverse life stages ofC. steinii, which are also corroborated inC. inflata. During the resting cyst stage, genes associated with cell death and vacuole formation are upregulated, and translation-related genes are downregulated. While the translation-related genes are upregulated during the excystment of resting cysts. Reproductive cysts exhibit a significant reduction in cell adhesion. We also demonstrate that most genes expressed in specific life stages are under strong purifying selection. This study offers a deeper understanding of the life history evolution that underpins the extraordinary success and ecological functions of microorganisms in soil ecosystems.IMPORTANCEColpodaspecies, as a prominent group among the most widely distributed and abundant soil microorganisms, play a crucial role in sustaining soil ecosystems and promoting plant growth. This investigation reveals their exceptional macronuclear genomic features, including significantly large genome size, long introns, and numerous gene duplications. The gene expression profiles and the specific biological functions associated with the transitions between various life stages are also elucidated. The vast majority of genes linked to life stage transitions are subject to strong purifying selection, as inferred from multiple natural strains newly isolated and deeply sequenced. This substantiates the enduring and conservative nature ofColpoda’s life history, which has persisted throughout the extensive evolutionary history of these highly successful protozoa in soil. These findings shed light on the evolutionary dynamics of microbial eukaryotes in the ever-fluctuating soil environments. This integrative research represents a significant advancement in understanding the life histories of these understudied single-celled eukaryotes. 

Colpoda, one of the most widespread ciliated protozoa in soil, are poorly understood in regard to their genetics and evolution. Our research revealed extreme mitochondrial gene rearrangements dominated by gene loss events, potentially leading to the streamlining ofColpodamitogenomes. Surprisingly, while interspecific rearrangements abound, our population-level mitogenomic study revealed a conserved gene order within species, offering a potential new identification criterion. Phylogenomic analysis traced their lineage over 326 million years, revealing two distinct groups. Substantial genomic divergence might be associated with the lack of extended collinear blocks and relaxed purifying selection. This study systematically revealsColpodaciliate mitogenome structures and evolution, providing insights into the survival and evolution of these vital soil microorganisms. 

Abstract Microbial strains with high genomic stability are particularly sought after for testing the quality of commercial microbiological products, such as biological media and antibiotics. Yet, using mutation–accumulation experiments and de novo assembled complete genomes based on Nanopore long-read sequencing, we find that the widely used quality-control strain Shewanella putrefaciens ATCC-8071, also a facultative pathogen, is a hypermutator, with a base-pair substitution mutation rate of 2.42 × 10−8 per nucleotide site per cell division, ∼146-fold greater than that of the wild-type strain CGMCC-1.6515. Using complementation experiments, we confirm that mutL dysfunction, which was a recent evolutionary event, is the cause for the high mutation rate of ATCC-8071. Further analyses also give insight into possible relationships between mutation and genome evolution in this important bacterium. This discovery of a well-known strain being a hypermutator necessitates screening the mutation rate of bacterial strains before any quality control or experiments.