Endosymbioses have shaped the evolutionary trajectory of life and remain ecologically important. Investigating oceanic photosymbioses can illuminate how algal endosymbionts are energetically exploited by their heterotrophic hosts and inform on putative initial steps of plastid acquisition in eukaryotes. By combining three-dimensional subcellular imaging with photophysiology, carbon flux imaging, and transcriptomics, we show that cell division of endosymbionts (Phaeocystis) is blocked within hosts (Acantharia) and that their cellular architecture and bioenergetic machinery are radically altered. Transcriptional evidence indicates that a nutrient-independent mechanism prevents symbiont cell division and decouples nuclear and plastid division. As endosymbiont plastids proliferate, the volume of the photosynthetic machinery volume increases 100-fold in correlation with the expansion of a reticular mitochondrial network in close proximity to plastids. Photosynthetic efficiency tends to increase with cell size, and photon propagation modeling indicates that the networked mitochondrial architecture enhances light capture. This is accompanied by 150-fold higher carbon uptake and up-regulation of genes involved in photosynthesis and carbon fixation, which, in conjunction with a ca.15-fold size increase of pyrenoids demonstrates enhanced primary production in symbiosis. Mass spectrometry imaging revealed major carbon allocation to plastids and transfer to the host cell. As in most photosymbioses, microalgae are contained within a host phagosome (symbiosome), but here, the phagosome invaginates into enlarged microalgal cells, perhaps to optimize metabolic exchange. This observation adds evidence that the algal metamorphosis is irreversible. Hosts, therefore, trigger and benefit from major bioenergetic remodeling of symbiotic microalgae with potential consequences for the oceanic carbon cycle. Unlike other photosymbioses, this interaction represents a so-called cytoklepty, which is a putative initial step toward plastid acquisition.

Summary Climate change scenarios predict tropical cyclones will increase in both frequency and intensity, which will escalate the amount of terrestrial run‐off and mechanical disruption affecting coastal ecosystems. Bacteria are key contributors to ecosystem functioning, but relatively little is known about how they respond to extreme storm events, particularly in nearshore subtropical regions. In this study, we combine field observations and mesocosm experiments to assess bacterial community dynamics and changes in physicochemical properties during early‐ and late‐season tropical cyclones affecting Okinawa, Japan. Storms caused large and fast influxes of freshwater and terrestrial sediment – locally known as red soil pollution – and caused moderate increases of macronutrients, especially SiO2 and PO43−, with up to 25 and 0.5 μM respectively. We detected shifts in relative abundances of marine and terrestrially derived bacteria, including putative coral and human pathogens, during storm events. Soil input alone did not substantially affect marine bacterial communities in mesocosms, indicating that other components of run‐off or other storm effects likely exert a larger influence on bacterial communities. The storm effects were short‐lived and bacterial communities quickly recovered following both storm events. The early‐ and late‐season storms caused different physicochemical and bacterial community changes, demonstrating the context‐dependency of extreme storm responses in a subtropical coastal ecosystem.

Acantharians (supergroup Rhizaria) can be important contributors to surface primary production and to carbon flux to the deep sea, but are often underestimated because their delicate structures are destroyed by plankton nets or dissolved by chemical fixatives. As they are also uncultured, relatively little is known about acantharian biology, especially regarding their life cycles. Here, we take a paired approach, bringing together high‐throughput, in situ imaging and metabarcode sequencing, to investigate acantharian abundance, vertical distribution, and life history in the western North Pacific. Concentrations of imaged acantharian cells correlated well with relative abundances of 18S rRNA gene sequences from acantharians with known, recognizable morphologies, but not to sequences corresponding to acantharians with unknown morphology. These results suggest that morphologically undescribed clades may lack the characteristic star‐shaped acantharian skeleton or are much smaller than described acantharians. The smaller size of acantharians imaged at depth supports current hypotheses regarding nonsymbiotic acantharian life cycles: cysts or vegetative cells release reproductive swarmer cells in deep water and juvenile cells grow as they ascend toward the surface. Moreover, sequencing data present the possibility that some photosymbiotic acantharians may also reproduce at depth, like their nonsymbiotic, encysting relatives, which is counter to previous hypotheses. Finally, in situ imaging captured a new acantharian behavior that may be a previously undescribed predation strategy.

Phaeocystis is a cosmopolitan, bloom-forming phytoplankton genus that contributes significantly to global carbon and sulfur cycles. During blooms, Phaeocystis species produce large carbon-rich colonies, creating a unique interface for bacterial interactions. While bacteria are known to interact with phytoplankton—e.g., they promote growth by producing phytohormones and vitamins—such interactions have not been shown for Phaeocystis. Therefore, we investigated the composition and function of P. globosa microbiomes. Specifically, we tested whether microbiome compositions are consistent across individual colonies from four P. globosa strains, whether similar microbiomes are re-recruited after antibiotic treatment, and how microbiomes affect P. globosa growth under limiting conditions. Results illuminated a core colonial P. globosa microbiome—including bacteria from the orders Alteromonadales, Burkholderiales, and Rhizobiales—that was re-recruited after microbiome disruption. Consistent microbiome composition and recruitment is indicative that P. globosa microbiomes are stable-state systems undergoing deterministic community assembly and suggests there are specific, beneficial interactions between Phaeocystis and bacteria. Growth experiments with axenic and nonaxenic cultures demonstrated that microbiomes allowed continued growth when B-vitamins were withheld, but that microbiomes accelerated culture collapse when nitrogen was withheld. In sum, this study reveals symbiotic and opportunistic interactions between Phaeocystis colonies and microbiome bacteria that could influence large-scale phytoplankton bloom dynamics and biogeochemical cycles.