Paired high‐throughput, in situ imaging and high‐throughput sequencing illuminate acantharian abundance and vertical distribution

Abstract

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.

Combining multi-marker metabarcoding and digital holography to describe eukaryotic plankton across the Newfoundland Shelf

“…Future studies investigating plankton size structure from the HoloSea or similar holographic microscopes should implement a correction factor to account for the scattering of coherent light that biases size estimates non-linearly depending on object distance from the point source 64 . The promise for digital in-line holography is shared by digital imaging technologies more broadly, and is typically prohibitive for conventional light microscopy, which is to yield data-rich, high-frequency observations which to date have captured planktonic fish-larvae survivorship under river plume discharge regimes 65 , the evolution of particulate-mediated carbon export in rapidly changing marginal zones 66 , spatial patterns in plankton community compositions through time 67 , at regional scales 4 , 68 and specific taxonomic lineages at global scales 69 . Novel biotic interactions have recently been observed using in-situ imaging, including pseudopodial feeding in acantharians from the East China Sea likely missed previously due to destructive sampling by conventional plankton nets 4 and the frequent parasitization of the cosmopolitan copepod Oithona at the Scripps Pier in the Pacific Ocean 70 .…”

“…The promise for digital in-line holography is shared by digital imaging technologies more broadly, and is typically prohibitive for conventional light microscopy, which is to yield data-rich, high-frequency observations which to date have captured planktonic fish-larvae survivorship under river plume discharge regimes 65 , the evolution of particulate-mediated carbon export in rapidly changing marginal zones 66 , spatial patterns in plankton community compositions through time 67 , at regional scales 4 , 68 and specific taxonomic lineages at global scales 69 . Novel biotic interactions have recently been observed using in-situ imaging, including pseudopodial feeding in acantharians from the East China Sea likely missed previously due to destructive sampling by conventional plankton nets 4 and the frequent parasitization of the cosmopolitan copepod Oithona at the Scripps Pier in the Pacific Ocean 70 . Digital imaging can also capture size-structure patterns as an indicator of functional diversity 71 , which is a deeply evolutionary trait that affects ocean food webs and biogeochemistry 72 , 73 .…”

“…Plankton monitoring tools using conventional microscopy are steadily being replaced by a new generation of optics in digital imaging instruments, equipped with algorithms to extract, store, and classify major plankton groups mostly within nano-mesoplankton (2 µm to 20 mm) size ranges and bearing morphologically distinct features 2 , 3 . Imaging provides quantitative observations of taxonomic and functional diversity while also capturing species behaviour with unintrusive, in-flow sampling designs 4 . Together, the enhanced sampling capacity and stored digital information in image data have tremendous potential for quantitative plankton ecology, especially for morphologically diverse eukaryotes 5 , 6 .…”

Environmental sequencing of marine protistan plankton communities reveals the effects of mesoscale cyclonic eddy transport on regional protistan diversity in subtropical offshore waters

“…Arthracanthida and Symphyacanthida complete their full life cycles in the photic zone because they are not capable of forming cysts and each new generation is forced to recruit new phototrophic endobionts (Decelle et al, 2013;Martin et al, 2010). Thus, their abundances typically decrease with water depth (Mars Brisbin et al, 2020). The 1989).…”

Diversity and ecology of Radiolaria in modern oceans

“…mostly ciliates and tintinnids) or even multicellular heterotrophs (e.g. copepods, large mollusc larvae; Anderson, 1977; Sugiyama and Anderson, 1998; Bernstein et al ., 1999; Matsuoka, 2007; Sugiyama et al ., 2008; Suzuki and Not, 2015; Mars Brisbin et al ., 2020). A few reports, however, indicate that some radiolarians could be detritivores (Anderson, 1983).…”