No abstract

Molecular analysis revealed diel rhythmicity in the metabolic activity of single-celled microbial eukaryotes (protists) within an eddy in the North Pacific Subtropical Gyre (ca. 100 km NE of station ALOHA). Diel trends among different protistan taxonomic groups reflected distinct nutritional capabilities and temporal niche partitioning. Changes in relative metabolic activities among phototrophs corresponded to the light cycle, generally peaking in mid-to late-afternoon. Metabolic activities of protistan taxa with phagotrophic ability were higher at night, relative to daytime, potentially in response to increased availability of picocyanobacterial prey. Tightly correlated Operational Taxonomic Units throughout the diel cycle implicated the existence of parasitic and mutualistic relationships within the microbial eukaryotic community, underscoring the need to define and include these symbiotic interactions in marine food web descriptions. This study provided a new high-resolution view into the ecologically important interactions among primary producers and consumers that mediate the transfer of carbon to higher trophic levels. Characterizations of the temporal dynamics of protistan activities contribute knowledge for predicting how these microorganisms respond to environmental forcing factors.

Kleptoplastidic, or chloroplast‐stealing, lineages offer insight into the process of acquiring photosynthesis. By quantifying the ability of these organisms to retain and use photosynthetic machinery from their prey, we can understand how intermediaries on the endosymbiosis pathway might have evolved regulatory and maintenance mechanisms. Here, we focus on a mixotrophic kleptoplastidic ciliate, Mesodinium chamaeleon, noteworthy for its ability to retain functional chloroplasts from at least half a dozen cryptophyte algal genera. We contrasted the performance of kleptoplastids from blue‐green and red cryptophyte prey as a function of light level and feeding history. Our experiments showed that starved M. chamaeleon cells are able to maintain photosynthetic function for at least 2 weeks and that M. chamaeleon containing red plastids lost chlorophyll and electron transport capacity faster than those containing blue‐green plastids. However, likely due to increased pigment content and photosynthetic rates in red plastids, M. chamaeleon had higher growth rates and more prolonged growth when feeding on red cryptophytes. For example, M. chamaeleon grew rapidly and extensively when fed the blue‐green cryptophyte Chroomonas mesostigmatica, but this growth appeared to hinge on high levels of feeding supporting photosynthetic activity. In contrast, even starved M. chamaeleon containing red plastids from Rhodomonas salina could achieve high photosynthetic rates and extensive growth. Our findings show that plastid origin impacts the maintenance and magnitude of photosynthetic activity, though whether this is due to variation in ciliate control or gradual loss of plastid function in ingested prey cells remains unknown.

Photosymbiotic protists contribute to surface primary production in low-nutrient, open-ocean ecosystems and constitute model systems for studying plastid acquisition via endosymbiosis. Little is known, however, about host-symbiont dynamics in these important relationships, and whether these symbioses are mutualistic is debated. In this study, we applied single-cell sequencing methods and advanced fluorescent microscopy to investigate host-symbiont dynamics in clade F acantharians, a major group of photosymbiotic protists in oligotrophic subtropical gyres. We amplified the 18S rRNA gene from single acantharian hosts and environmental samples to assess intra-host symbiont diversity and to determine whether intra-host symbiont community composition directly reflects the available symbiont community in the surrounding environment. Our results demonstrate that clade F acantharians simultaneously host multiple species from the haptophyte genera Phaeocystis and Chrysochromulina. The intra-host symbiont community composition was distinct from the external free-living symbiont community, suggesting that these acantharians maintain symbionts for extended periods of time. After selectively staining digestive organelles, fluorescent confocal microscopy showed that symbionts were not being systematically digested, which is consistent with extended symbiont maintenance within hosts. Extended maintenance within hosts may benefit symbionts through protection from grazing or viral lysis, and therefore could enhance dispersal, provided that symbionts retain reproductive capacity. The evidence for extended symbiont maintenance therefore allows that Phaeocystis could glean some advantage from the symbiosis and leaves the possibility of mutualism.

Radiolarians are a group of ubiquitous, yet poorly understood, large protists that often harbor photosymbionts. We studied the solitary radiolarian Thalassicolla nucleata by analyzing the transcriptome of its holobiont. We found that T. nucleata contained two dinoflagellate symbionts, one photosymbiont Brandtodinium sp., and one putative Peridiniales parasite. Through comparisons of gene expressions of Brandtodinium sp. and those of a close relative from a free-living culture, we found that the Brandtodinium sp. maintained its photosynthetic activities, but altered its carbon metabolism dramatically in hospite. Gene expression data also suggested carbon and nitrogen exchange between the host and photosymbiont and that lectin-glycan interaction might play an important role in host-symbiont recognition.

The extent to which animals can regenerate cells, tissues, or body parts varies largely. Hydra has a remarkable ability to undergo full body regeneration. Bisected polyps can regenerate the head and foot, and whole polyps can form from aggregates of cells. This capability is made possible by a cluster of cells known as the head organizer. This organizer has the capability to self-regulate and to induce a second axis. Previous studies have found Wnt3 and other developmental genes associated with head organizer function. Yet, the cellular composition and molecular program of regenerating tissue remains largely unknown. In this study, we used single cell RNA-seq from a regeneration time course to identify the molecular and cellular features of Hydra head regeneration. We identified nine distinct cell types in the regenerating head tissue, including candidate head organizer cells. We found Wnt-signaling and early wound response genes co-expressed with Wnt3, and all were more highly expressed in the head organizer cell cluster. In addition, we found that Wnt3 expression is likely being regulated by conserved developmental transcription factors. Our study reveals coordination of early wound response, developmental transcription factors, and transposable elements during Hydra tissue regeneration and provides insight into the evolution of development and regeneration programs.

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