The microbiome of the Arctic planktonic foraminifera Neogloboquadrina pachyderma is composed of fermenting and carbohydrate-degrading bacteria and an intracellular diatom chloroplast store

Abstract

Neogloboquadrina pachyderma is the only true polar species of planktonic foraminifera. As a key component of the calcite flux, it plays a crucial role in the reconstruction and modelling of seasonality and environmental change within the high latitudes. The rapidly changing environment of the polar regions of the North Atlantic and Arctic oceans poses challenging conditions for this (sub)polar species in terms of temperature, sea-ice decline, calcite saturation, ocean pH, and the progressive contraction of the polar ecosystem. To model the potential future for this important high-latitude species, it is vital to investigate the modern ocean community structure throughout the annual cycle of the Arctic to understand the inter-dependencies of N. pachyderma. This study focusses on the summer ice-free populations in Baffin Bay. We use 16S rDNA metabarcoding and transmission electron microscopy (TEM) to identify the microbial interactions of N. pachyderma and PICRUSt2 to predict the metabolic pathways represented by the amplicon sequencing variants (ASVs) in the foraminiferal microbiome. We demonstrate that the N. pachyderma diet consists of both diatoms and bacteria. The core microbiome, defined as the 16S rDNA ASVs found in 80 % of the individuals investigated, consists of six bacterial ASVs and two diatom chloroplast ASVs. On average, it accounts for nearly 50 % of the total ASVs in any individual. The metabolic pathway predictions based on bacterial ASVs suggest that the foraminiferal microbiome is composed of monosaccharide fermenting and polysaccharide degrading bacterial species in line with those found routinely in the diatom phycosphere. On average, the two chloroplast ASVs constitute 40 % of the core microbiome, and, significantly, an average of 53.3 % of all ASVs in any individual are of chloroplast origin. TEM highlights the importance of diatoms to this species by revealing that intact chloroplasts remain in the foraminiferal cytoplasm in numbers strikingly comparable to the substantial quantities observed in kleptoplastic benthic foraminifera. Diatoms are the major source of kleptoplasts in benthic foraminifera and other kleptoplastic groups, but this adaptation has never been observed in a planktonic foraminifer. Further work is required to understand the association between N. pachyderma, diatoms, and their chloroplasts in the pelagic Arctic realm, but such a strategy may confer an advantage to this species for survival in this extreme habitat.