Significance: The marine unicellular cyanobacterium Prochlorococcus is the most abundant photosynthetic organism on Earth. Members of this genus are classically thought to be adapted to high-oxygen and nutrient-poor ocean conditions, with a principle divergence between high-light and low-light ecotypes. We show that the most basal Prochlorococcus lineages are adapted to the low-oxygen, low-light, and high-nutrient conditions found in the dimly illuminated waters of anoxic marine zones. The most basal lineages have retained phycobilisomes as light-harvesting antennae—a characteristic of most other cyanobacteria—whose loss was thought to define all Prochlorococcus . As oxygenic photosynthesis drove ocean oxidation in the ancient Earth, oxygen appears to have played as much a role as light and nutrients in driving Prochlorococcus evolution.

Little is still known of the impacts of protist grazing on bacterioplankton communities in the dark ocean. Furthermore, the accuracy of assessments of in situ microbial activities, including protist grazing, can be affected by sampling artifacts introduced during sample retrieval and downstream manipulations. Potential artifacts may be increased when working with deep-sea samples or samples from chemically unique water columns such as oxygen minimum zones (OMZs). OMZs are oxygen-depleted regions in the ocean, where oxygen concentrations can drop to <20 µM. These regions are typically located near eastern boundary upwelling systems and currently occur in waters occupying below about 8% of total ocean surface area, representing ~1% of the ocean’s volume. OMZs have a profound impact not only on the distribution of marine Metazoa, but also on the composition and activities of microbial communities at the base of marine food webs. Here we present an overview of current knowledge of protist phagotrophy below the photic zone, emphasizing studies of oxygen-depleted waters and presenting results of the first attempt to implement new technology for conducting these incubation studies completely in situ (the Microbial Sampling- Submersible Incubation Device, MS-SID). We performed 24-h incubation experiments in the Eastern Tropical South Pacific (ETSP) OMZ. This preliminary study shows that up to 28% of bacterial biomass may be consumed by protists in waters where oxygen concentrations were down to ~3 µM and up to 13% of saturation at a station with nitrate accumulation where oxygen concentrations were undetectable. Results also show that shipboard measurements of grazing rates were lower than rates measured from the same water using the MS-SID, suggesting that in situ experiments help to minimize artifacts that may be introduced when conducting incubation studies using waters collected from below the photic zone, particularly from oxygen-depleted regions of the water column.

Prochlorococcus and Synechococcus are the most abundant free‐living photosynthetic microorganisms in the ocean. Uncultivated lineages of these picocyanobacteria also thrive in the dimly illuminated upper part of oxygen‐deficient zones (ODZs), where an important portion of ocean nitrogen (N) loss takes place via denitrification and anaerobic ammonium oxidation. Recent metagenomic studies revealed that ODZ Prochlorococcus have the genetic potential for using different N forms, including nitrate and nitrite, uncommon N sources for Prochlorococcus, but common for Synechococcus. To determine which N sources ODZ picocyanobacteria are actually using in nature, the cellular ¹⁵N natural abundance (δ¹⁵N) and assimilation rates of different N compounds were determined using cell sorting by flow cytometry and mass spectrometry. The natural δ¹⁵N of the ODZ Prochlorococcus varied from −4.0‰ to 13.0‰ (n = 9), with 50% of the values in the range of −2.1–2.6‰. While the highest values suggest nitrate use, most observations indicate the use of nitrite, ammonium, or a mixture of N sources. Meanwhile, incubation experiments revealed potential assimilation rates of ammonium and urea in the same order of magnitude as that expected for total N in several environments including ODZs, whereas rates of nitrite and nitrate assimilation were very low. Our results thus indicate that reduced forms of N and nitrite are the dominant sources for ODZ picocyanobacteria, although nitrate might be important on some occasions. ODZ picocyanobacteria might thus represent potential competitors with anammox bacteria for ammonium and nitrite, with ammonia‐oxidizing archaea for ammonium, and with nitrite‐oxidizing bacteria for nitrite.

Gammaproteobacteria of the genus Alteromonas are prominent members of pelagic marine microbial communities, playing critical roles in the aerobic degradation of particulate organic matter. Comparative genomic studies of these microorganisms have mainly focused on the metabolic and genomic plasticity of strains isolated primarily from oxygenated environments. In this study, we show that Alteromonas significantly contribute to marine microbial communities from suboxic waters ([O₂] < 5 uM) in both the free-living (FL) and particle-attached (PA) fractions, but considerably decrease in abundance in the anoxic waters. The highest proportion of Alteromonas transcripts was found within the secondary fluorescence maximum (SFM) of Oxygen Minimum Zones (OMZs). This metatranscriptomic information suggests an in situ coupling of Alteromonas iron (Fe) and carbon metabolisms, and a relevant role of the glyoxylate cycle across the different layers of the OMZs. This study demonstrates that Alteromonas is an abundant and active member of the OMZ microbial communities, with a potentially significant impact on the carbon cycling in these ecosystems. These results provide valuable environmental evidence to support previous culture-based studies assessing the physiology and ecology of these ubiquitous marine heterotrophs under low-oxygen conditions.

Hypersaline environments represent some of the most challenging settings for life on Earth. Extremely halophilic microorganisms have been selected to colonize and thrive in these extreme environments by virtue of a broad spectrum of adaptations to counter high salinity and osmotic stress. Although there is substantial data on microbial taxonomic diversity in these challenging ecosystems and their primary osmoadaptation mechanisms, less is known about how hypersaline environments shape the genomes of microbial inhabitants at the functional level. In this study, we analyzed the microbial communities in five ponds along the discontinuous salinity gradient from brackish to salt-saturated environments and sequenced the metagenome of the salt (halite) precipitation pond in the artisanal Cáhuil Solar Saltern system. We combined field measurements with spectrophotometric pigment analysis and flow cytometry to characterize the microbial ecology of the pond ecosystems, including primary producers and applied metagenomic sequencing for analysis of archaeal and bacterial taxonomic diversity of the salt crystallizer harvest pond. Comparative metagenomic analysis of the Cáhuil salt crystallizer pond against microbial communities from other salt-saturated aquatic environments revealed a dominance of the archaeal genus Halorubrum and showed an unexpectedly low abundance of Haloquadratum in the Cáhuil system. Functional comparison of 26 hypersaline microbial metagenomes revealed a high proportion of sequences associated with nucleotide excision repair, helicases, replication and restriction-methylation systems in all of them. Moreover, we found distinctive functional signatures between the microbial communities from salt-saturated (>30% [w/v] total salinity) compared to sub-saturated hypersaline environments mainly due to a higher representation of sequences related to replication, recombination and DNA repair in the former. The current study expands our understanding of the diversity and distribution of halophilic microbial populations inhabiting salt-saturated habitats and the functional attributes that sustain them.

Cáhuil Lagoon in central Chile harbors distinct microbial communities in various solar salterns that are arranged as interconnected ponds with increasing salt concentrations. Here, we report the metagenome of the 3.0- to 0.2-µm fraction of the microbial community present in a crystallizer pond with 34% salinity.