Summary The transcriptomic responses of bacteria to environmental stresses have been studied extensively, yet we know little about how the stressed cells respond to bacteriophage infection. Here, we conducted the first whole transcriptome sequencing (RNA‐seq) study of stressed bacteria to phage infection by infecting the marine picocyanobacterium Prochlorococcus NATL2A with cyanomyovirus P‐SSM2 under P limitation, a strong selective force in the oceans. Transcripts of the P‐acquisition genes in the uninfected cells were enriched after P limitation, including the high‐affinity phosphate‐binding protein gene pstS. They were still enriched in the infected cells under P‐limited conditions. In contrast, transcripts of adenosine triphosphate (ATP) synthase and ribosomal protein genes were depleted in the uninfected cells after P limitation but were enriched during phage infection of P‐starved cells. Cyanophage P‐SSM2 contains pstS, and pstS and its adjacent gene g247 of unknown function were the only phage genes that were enriched under P‐limited conditions. We further found that the host pstS transcript number per cell decreased after infection, however, it was still much higher in the P‐limited infected cells than that in the nutrient‐replete cells. Moreover, phage pstS transcript number per cell was ∼20 times higher than the host copy, which may help maintain the host phosphate uptake rate during infection.

MicroRNAs (miRNAs) and endogenous small interfering RNAs (siRNAs) are key players in plant stress responses. Here, we present the sRNA transcriptomes of mangroves Bruguiera gymnorrhiza and Kandelia candel. Comparative computational analyses and target predictions revealed that mangroves exhibit distinct sRNA regulatory networks that differ from those of glycophytes. A total of 32 known and three novel miRNA families were identified. Conserved and mangrove-specific miRNA targets were predicted; the latter were widely involved in stress responses. The known miRNAs showed differential expression between the mangroves and glycophytes, reminiscent of the adaptive stress-responsive changes in Arabidopsis. B. gymnorrhiza possessed highly abundant but less conserved TAS3 trans-acting siRNAs (tasiRNAs) in addition to tasiR-ARFs, with expanded potential targets. Our results indicate that the evolutionary alteration of sRNA expression levels and the rewiring of sRNA-regulatory networks are important mechanisms underlying stress adaptation. We also identified sRNAs that are involved in salt and/or drought tolerance and nutrient homeostasis as possible contributors to mangrove success in stressful environments.

A drop of seawater contains numerous microspatial niches at the scale relevant to microbial activities. Examples are abiotic niches such as detrital particles that show different sizes and organic contents, and biotic niches resulting from bacteria–phage and bacteria–phytoplankton interactions. A common practice to investigate the impact of microenvironments on bacterial evolution is to separate the microenvironments physically and compare the bacterial inhabitants from each. It remains poorly understood, however, which microenvironment primarily drives bacterioplankton evolution in the pelagic ocean. By applying a dilution cultivation approach to an undisturbed coastal water sample, we isolate a bacterial population affiliated with the globally dominant Roseobacter group. Although varying at just a few thousand nucleotide sites across the whole genomes, members of this clonal population are diverging into two genetically separated subspecies. Genes underlying speciation are not unique to subspecies but instead clustered at the shared regions that represent ~6% of the genomic DNA. They are primarily involved in vitamin synthesis, motility, oxidative defense, carbohydrate, and amino acid utilization, consistent with the known strategies that roseobacters take to interact with phytoplankton and particles. Physiological assays corroborate that one subspecies outcompetes the other in these traits. Our results indicate that the microenvironments in the pelagic ocean represented by phytoplankton and organic particles are likely important niches that drive the cryptic speciation of the Roseobacter population, though microhabitats contributed by other less abundant pelagic hosts cannot be ruled out.

Phytoplankton contribute almost half of the world's total primary production. The exudates and viral lysates of phytoplankton are two important forms of dissolved organic matter (DOM) in aquatic environments and fuel heterotrophic prokaryotic metabolism. However, the effect of viral infection on the composition and biological availability of phytoplankton-released DOM is poorly understood. Here, we investigated the optical characteristics and microbial utilization of the exudates and viral lysates of the ecologically important unicellular picophytoplankton Prochlorococcus. Our results showed that Prochlorococcus DOM produced by viral lysis (Pro-vDOM) with phages of three different morphotypes (myovirus P-HM2, siphovirus P-HS2 and podovirus P-SSP7) had higher humic-like fluorescence intensities, lower absorption coefficients and higher spectral slopes compared to DOM exuded by Prochlorococcus (Pro-exudate). The results indicate that viral infection altered the composition of Prochlorococcus-derived DOM and might contribute to the pool of oceanic humic-like DOM. Incubation with Pro-vDOM resulted in a greater dissolved organic carbon (DOC) degradation rate and decreases in the absorption spectral slope and heterotrophic bacterial growth rate compared to incubation with Pro-exudate, suggesting that Pro-vDOM was more bioavailable compared to Pro-exudate. In addition, the stimulated microbial community succession trajectories were significantly different between the Pro-exudate and Pro-vDOM treatments, indicating that viral lysates play an important role in shaping the heterotrophic bacterial community. Our study demonstrated that viral lysis altered the chemical composition and biological availability of DOM derived from Prochlorococcus, which is the numerically dominant phytoplankton in the oligotrophic ocean. Importance The unicellular picocyanobacterium Prochlorococcus is the numerically dominate phytoplankton in the oligotrophic ocean, contributing to the vast majority of marine primary production. Prochlorococcus releases a significant fraction of fixed organic matter into surrounding environment and supports a vital portion of heterotrophic bacterial activity. Viral lysis is an important biomass loss process of Prochlorococcus. Yet little is known about whether and how viral lysis affects Prochlorococcus-released dissolved organic matter (DOM). Our paper shows that viral infection alters the optical properties (such as the absorption coefficients, spectral slopes and fluorescence intensities) of released DOM and might contribute to a humic-like DOM pool and carbon sequestration in the ocean. Meanwhile, viral lysis also releases various intracellular labile DOM including amino acids, protein-like DOM and lower-molecular weight DOM, increases the bioavailability of DOM and shapes the successive trajectory of the heterotrophic bacterial community. Our study highlights the importance of viruses in impacting the DOM quality in the ocean.