Logan M. Peoples

Oceanic microorganisms can rapidly respond to environmental variability. Determining how physical and biological processes control microbial distributions, abundances, and metabolic dynamics is challenging. Here, we used autonomous underwater vehicles capable of Lagrangian feature tracking and in situ sampling, in combination with ship-based measurements, to examine diel to weekly scale changes in microbial transcription and biogeochemistry in the deep chlorophyll maximum (DCM) of a mesoscale cyclonic eddy. Nearly 20% of total transcript expression showed diel periodicity, highlighting the importance of the diurnal cycle on phytoplankton metabolism in the dim waters of the DCM. Eddy-induced isopycnal uplift increased nutrient concentrations and caused upward displacement of the DCM, driving increased picoeukaryotic cell abundances and transcriptional activity of nitrate-incorporating photoautotrophs. As the eddy weakened, the DCM deepened and transcriptional activity shifted towards chemolithoautotrophic ammonia-oxidizing archaea. The temporal dynamics observed demonstrate how plankton communities rapidly respond to both diel variation and stochastic mesoscale disturbances.

Three species of snailfishes (family Liparidae) are described from single collections based on morphological and genetic evidence, from the eastern abyssal Pacific, depths 3,268–4,119 m. Careproctus colliculi, new species, the Bumpy Snailfish, can be identified by its pink color in life, 22 pectoral-fin rays (uppermost rays long), round head, eight caudal rays, large eye, and well-developed pterygiophores that form a large suction disk. Careproctus yanceyi, new species, the Dark Snailfish, bears a moderate ventral suction disk (<3% standard length), single nostrils, six branchiostegal rays, and is distinct from other eastern Pacific deepwater snailfishes in having a fully black body with a rounded head and horizontal mouth. Additional defining characters include a small gill opening located entirely above the pectoral fin, two pectoral radials, and 22 pectoral-fin rays. Paraliparis em, new species, the Sleek Snailfish, is distinguished from other snailfishes by its long, black, laterally compressed body, absence of a suction disk, prominently angled jaw, single pectoral-fin radial, anteriorly positioned anus, and five branchiostegal rays. Each of these three taxa has a distinct mitochondrial cytochrome c oxidase subunit I (COI) sequence compared to all other sequenced snailfishes. Genetically, Paraliparis em, new species, is most similar to P. wolffi from the Crozet Basin in the Indian Ocean, as well as bearing similarity to the northeastern Pacific snailfishes P. megalopus and P. ulochir, together known as Paraliparis Clade I. Careproctus yanceyi, new species, shows little similarity in COI sequences to other taxa and perhaps represents a distinct clade in the family. The COI sequence of Careproctus colliculi, new species, fits in the Osteocareprocta clade, most similar to Careproctus continentalis, C. discoveryae, C. longipectoralis, and Osteodiscus cascadiae. Paraliparis em, new species, and Careproctus yanceyi, new species, show significant morphological and genetic divergence from one another, despite both being black snailfishes collected on the same submersible dive. These findings reveal cryptic diversity in deep-sea snailfishes and highlight the necessity of combined imaging, morphological, and genetic approaches to studying fish biodiversity. These three newly discovered species begin to fill an important sampling gap for the family Liparidae and demonstrate the importance of snailfishes in communities of the abyssal seafloor.

Glaciers are retreating, altering alpine ecosystems and creating new proglacial lakes. Compared to lakes fed by snowpack, glacial lakes are often enriched in nutrients and suspended solids that decrease light penetration. However, the microorganisms and biogeochemical conditions within these newly formed lakes are not well characterized. We describe the microbial communities in 14 glacial lakes in Glacier National Park, MT, USA using 16S rRNA gene amplicon sequencing and measurements of nutrient concentrations, water clarity, and other environmental properties. Microbial communities were distinct between lakes, including those connected to the same glacier, indicating the importance of site-specific biogeochemical and physical dynamics on these systems. Microbial community composition correlated with lake age (formation before or after the Little Ice Age) and conductivity but not with whether a lake was connected to a contemporaneous glacier > 0.1 km2. Heterotrophic lineages found in other glacial systems were abundant and widespread, while cyanobacteria only reached appreciable abundances in shallow lakes where light reached the benthos. Relative abundances of ammonia and nitrite oxidizers correlated with concentrations of nitrate and nitrite, suggesting nitrification may help control nitrogen forms and concentrations in glacial lakes. We show that as glaciers recede, unique glacial lake microbial communities will be formed and lost with them.

Most deep-ocean life relies on organic carbon from the surface ocean. While settling primary production rapidly attenuates in the water column, pulses of organic material can be quickly transported to depth in the form of food falls. One example of fresh material that can reach great depths across the tropical Atlantic Ocean and Caribbean Sea is the pelagic macroalgae Sargassum . However, little is known about the deep-ocean organisms able to use this food source. Here, we encountered the isopod Bathyopsurus nybelini at depths 5002–6288 m in the Puerto Rico Trench and Mid-Cayman Spreading Center using the Deep Submergence Vehicle Alvin . In most of the 32 observations, the isopods carried fronds of Sargassum . Through an integrative suite of morphological, DNA sequencing, and microbiological approaches, we show that this species is adapted to feed on Sargassum by using a specialized swimming stroke, having serrated and grinding mouthparts, and containing a gut microbiome that provides a dietary contribution through the degradation of macroalgal polysaccharides and fixing nitrogen. The isopod’s physiological, morphological, and ecological adaptations demonstrate that vertical deposition of Sargassum is a direct trophic link between the surface and deep ocean and that some deep-sea organisms are poised to use this material.

Microorganisms grow despite imbalances in the availability of nutrients and energy. The biochemical and elemental adjustments that bacteria employ to sustain growth when these resources are suboptimal are not well understood. We assessed how Pseudomonas putida KT2440 adjusts its physiology at differing dilution rates (to approximate growth rates) in response to carbon (C), nitrogen (N), and phosphorus (P) stress using chemostats. Cellular elemental and biomolecular pools were variable in response to different limiting resources at a slow dilution rate of 0.12 h ⁻¹ , but these pools were more similar across treatments at a faster rate of 0.48 h ⁻¹ . At slow dilution rates, limitation by P and C appeared to alter cell growth efficiencies as reflected by changes in cellular C quotas and rates of oxygen consumption, both of which were highest under P- and lowest under C- stress. Underlying these phenotypic changes was differential gene expression of terminal oxidases used for ATP generation that allows for increased energy generation efficiency. In all treatments under fast dilution rates, KT2440 formed aggregates and biofilms, a physiological response that hindered an accurate assessment of growth rate, but which could serve as a mechanism that allows cells to remain in conditions where growth is favorable. Our findings highlight the ways that microorganisms dynamically adjust their physiology under different resource supply conditions, with distinct mechanisms depending on the limiting resource at slow growth and convergence toward an aggregative phenotype with similar compositions under conditions that attempt to force fast growth. IMPORTANCE: All organisms experience suboptimal growth conditions due to low nutrient and energy availability. Their ability to survive and reproduce under such conditions determines their evolutionary fitness. By imposing suboptimal resource ratios under different dilution rates on the model organism Pseudomonas putida KT2440, we show that this bacterium dynamically adjusts its elemental composition, morphology, pools of biomolecules, and levels of gene expression. By examining the ability of bacteria to respond to C:N:P imbalance, we can begin to understand how stoichiometric flexibility manifests at the cellular level and impacts the flow of energy and elements through ecosystems.

In oligotrophic oceans, the smallest eukaryotic phytoplankton are both significant primary producers and predators of abundant bacteria such as Prochlorococcus . However, the drivers and consequences of community dynamics among these diverse protists are not well understood. Here, we investigated how trophic strategies along the autotrophy‐mixotrophy spectrum vary in importance over time and across depths at Station ALOHA in the North Pacific Subtropical Gyre. We combined picoeukaryote community composition from a 28‐month time‐series with traits of diverse phytoplankton isolates from the same location, to examine trophic strategies across 13 operational taxonomic units and 8 taxonomic classes. We found that autotrophs and slower‐grazing mixotrophs tended to prevail deeper in the photic zone, while the most voracious mixotrophs were relatively abundant near the surface. Within the mixed layer, there was greater phagotrophy when conditions were most stratified and when Chl a concentrations were lowest, although the greatest temporal variation in trophic strategy occurred at intermediate depths (45–100 m). Dynamics at this site are consistent with previously described spatial patterns of trophic strategies. The success of relatively phagotrophic phytoplankton at shallower depths in the most stratified waters suggests that phagotrophy is a competitive strategy for acquiring nutrients when energy from light is plentiful.

Nitrification is an important control on the form and distribution of nitrogen in freshwater ecosystems. However, the seasonality of nitrogen pools and the diversity of organisms catalyzing this process have not been well documented in oligotrophic lakes. Here, we show that nitrogen pools and nitrifying organisms in Flathead Lake are temporally and vertically dynamic, with nitrifiers displaying specific preferences depending on the season. While the ammonia‐oxidizing bacteria (AOB) Nitrosomonadaceae and nitrite‐oxidizing bacteria (NOB) Nitrotoga dominate at depth in the summer, the ammonia‐oxidizing archaea (AOA) Nitrososphaerota and NOB Nitrospirota become abundant in the winter. Given clear seasonality in ammonium, with higher concentrations during the summer, we hypothesize that the succession between these two nitrifying groups may be due to nitrogen affinity, with AOB more competitive when ammonia concentrations are higher and AOA when they are lower. Nitrifiers in Flathead Lake share more than 99% average nucleotide identity with those reported in other North American lakes but are distinct from those in Europe and Asia, indicating a role for geographic isolation as a factor controlling speciation among nitrifiers. Our study shows there are seasonal shifts in nitrogen pools and nitrifying populations, highlighting the dynamic spatial and temporal nature of nitrogen cycling in freshwater ecosystems.

Temperate lakes experience variation in mixing and stratification that affects the distributions, activities, abundances, and diversity of plankton communities. We examined temporal and vertical changes in the composition of planktonic microorganisms (including Bacteria and Archaea) in oligotrophic Flathead Lake, Montana. Using a combination of approaches that included 16S rRNA gene sequencing and flow cytometric determination of cell abundances, we found that the microbial community was responsive to variations in stratification and mixing at time scales ranging from episodic (scale of days) to seasonal. However, the impact of such physical dynamics varied among taxa, likely reflecting taxa‐specific responses to environmental changes that coincide with stratification and mixing (e.g., light availability and nutrient supply). During the early spring, periods of relatively short‐term (< 7 d) intermittency in stratification and mixing influenced the vertical distributions of specific microbial taxa, notably including the cyanobacteria. These events highlight time scales of biological responses to high‐frequency variations associated with lake stratification and mixing, particularly during the transition to the growing season in the early spring.

With the ongoing differential disruption of the biogeochemical cycles of major elements that are essential for all life (carbon, nitrogen, and phosphorus), organisms are increasingly faced with a heterogenous supply of these elements in nature. Given that photosynthetic primary producers form the base of aquatic food webs, impacts of changed elemental supply on these organisms are particularly important. One way that phytoplankton cope with the differential availability of nutrients is through physiological changes, resulting in plasticity in macromolecular and elemental biomass composition. Here, we assessed how the green alga Chlamydomonas reinhardtii adjusts its macromolecular (e.g., carbohydrates, lipids, and proteins) and elemental (C, N, and P) biomass pools in response to changes in growth rate and the modification of resources (nutrients and light). We observed that Chlamydomonas exhibits considerable plasticity in elemental composition (e.g., molar ratios ranging from 124 to 971 for C:P, 4.5 to 25.9 for C:N, and 15.1 to 61.2 for N:P) under all tested conditions, pointing to the adaptive potential of Chlamydomonas in a changing environment. Exposure to low light modified the elemental and macromolecular composition of cells differently than limitation by nutrients. These observed differences, with potential consequences for higher trophic levels, included smaller cells, shifts in C:N and C:P ratios (due to proportionally greater N and P contents), and differential allocation of C among macromolecular pools (proportionally more lipids than carbohydrates) with different energetic value. However, substantial pools of N and P remained unaccounted for, especially at fast growth, indicating accumulation of N and P in forms we did not measure.

While methane is typically produced under anoxic conditions, methane supersaturation in the presence of oxygen has been observed in both marine and fresh waters. The biological cleavage of methylphosphonate (MPn), which releases both phosphate and methane, is one pathway that may contribute to this paradox. Here, we explore the genomic and functional potential for oxic methane production (OMP) via MPn in Flathead Lake, a large oligotrophic freshwater lake in northwest Montana. Time series and depth profile measurements show that epilimnetic methane was persistently supersaturated despite high oxygen levels, suggesting a possible in situ oxic source. Metagenomic sequencing indicated that 10% of microorganisms in the lake, many of which are related to the Burkholderiales (Betaproteobacteria) and Actinomycetota, have the genomic capacity to cleave MPn. We experimentally demonstrated that these organisms produce methane stoichiometrically with MPn consumption across multiple years. However, methane was only produced at appreciable rates in the presence of MPn when a labile organic carbon source was added, suggesting that this process may be limited by both MPn and labile carbon supply. Members of the genera Acidovorax , Rhodoferax , and Allorhizobium , organisms which make up less than 1% of Flathead Lake communities, consistently responded to MPn addition. We demonstrate that the genomic and physiological potential for MPn use exists among diverse, resident members of Flathead Lake and could contribute to OMP in freshwater lakes when substrates are available. IMPORTANCE: Methane is an important greenhouse gas that is typically produced under anoxic conditions. We show that methane is supersaturated in a large oligotrophic lake despite the presence of oxygen. Metagenomic sequencing indicates that diverse, widespread microorganisms may contribute to the oxic production of methane through the cleavage of methylphosphonate. We experimentally demonstrate that these organisms, especially members of the genus Acidovorax , can produce methane through this process. However, appreciable rates of methane production only occurred when both methylphosphonate and labile sources of carbon were added, indicating that this process may be limited to specific niches and may not be completely responsible for methane concentrations in Flathead Lake. This work adds to our understanding of methane dynamics by describing the organisms and the rates at which they can produce methane through an oxic pathway in a representative oligotrophic lake.