Metabarcoding Insights Into the Trophic Behavior and Identity of Intertidal Benthic Foraminifera

Abstract

Foraminifera are ubiquitous marine protists with an important role in the benthic carbon cycle. However, morphological observations often fail to resolve their exact taxonomic placement and there is a lack of field studies on their particular trophic preferences. Here, we propose the application of metabarcoding as a tool for the elucidation of the in situ feeding behavior of benthic foraminifera, while also allowing the correct taxonomic assignment of the feeder, using the V9 region of the 18S (small subunit; SSU) rRNA gene. Living foraminiferal specimens were collected from two intertidal mudflats of the Wadden Sea and DNA was extracted from foraminiferal individuals and from the surrounding sediments. Molecular analysis allowed us to confirm that our foraminiferal specimens belong to three genetic types: Ammonia sp. T6, Elphidium sp. S5 and Haynesina sp. S16. Foraminiferal intracellular eukaryote communities reflected to an extent those of the surrounding sediments but at different relative abundances. Unlike sediment eukaryote communities, which were largely determined by the sampling site, foraminiferal intracellular eukaryote communities were driven by foraminiferal species, followed by sediment depth. Our data suggests that Ammonia sp. T6 can predate on metazoan classes, whereas Elphidium sp. S5 and Haynesina sp. S16 are more likely to ingest diatoms. These observations, alongside the use of metabarcoding in similar ecological studies, significantly contribute to our overall understanding of the ecological roles of these protists in intertidal benthic environments and their position and function in the benthic food webs.

Enrichment of intracellular sulphur cycle –associated bacteria in intertidal benthic foraminifera revealed by 16S and aprA gene analysis

“…However, bacterial uptake by benthic foraminifera has been shown to be unselective, implying that bacterivory occurs mainly in association with potential deposit-feeding behaviour 21 . Feeding strategies, as well as organic matter turnover rates, appear to be species-specific 21–23 . For example, in situ experiments with 15 N labelled bacteria have shown that benthic foraminifer Ammonia tepida prefers algae in its diet over bacteria 24 , suggesting that bacteria are not its primary food source.…”

“…For example, in situ experiments with 15 N labelled bacteria have shown that benthic foraminifer Ammonia tepida prefers algae in its diet over bacteria 24 , suggesting that bacteria are not its primary food source. In addition to bacterivory, foraminifera are known to have a variety of other feeding strategies, such as herbivory, carnivory and even direct dissolved organic carbon uptake 21,23,25,26 . Mixotrophy is also an important trophic strategy for some shallow-water benthic foraminifera with the ability to harbour photosymbionts or kleptoplasts 27–29 .…”

“…(S5), and Haynesina sp. (S16) 23 collected from intertidal localities in the Dutch Wadden Sea. We compare the 16S rDNA metabarcoding –derived intracellular bacterial operational taxonomic units (OTUs) to those of the ambient sediment to determine which bacterial groups are enriched within foraminifera, and link the findings to sediment porewater chemistry and sediment bacteria distribution.…”

Foraminiferal community response to seasonal anoxia in Lake Grevelingen (the Netherlands)

“…Foraminifera exhibit a large range of feeding strategies, some are selective feeders (Muller, 1975;Suhr et al, 2003;Chronopoulou et al, 2019). Hagens et al (2015) reported that in Lake Grevelingen the phytoplankton composition was different between spring and summer 2012.…”

“…seems able to feed on very diverse food sources including microalgae, diatoms, bacteria or even metazoans (Lee et al, 1969;Moodley et al, 2000;Dupuy et al, 2010;Jauffrais et al, 2016;Chronopoulou et al, 2019). Recently, Chronopoulou et al (2019) showed different feeding preferences for Ammonia sp. T6 and E. selseyense in intertidal environments in the Dutch Wadden Sea.…”