Abstract
Abstract. We investigated the possibility of bacterial symbiosis in Globigerina bulloides, a palaeoceanographically important, planktonic foraminifer. This marine protist is commonly used in micropalaeontological investigations of climatically sensitive subpolar and temperate water masses as well as wind-driven upwelling regions of the world's oceans. G. bulloides is unusual because it lacks the protist algal symbionts that are often found in other spinose species. In addition, it has a large offset in its stable carbon and oxygen isotopic compositions compared to other planktonic foraminifer species, and also that predicted from seawater equilibrium. This is suggestive of novel differences in ecology and life history of G. bulloides, making it a good candidate for investigating the potential for bacterial symbiosis as a contributory factor influencing shell calcification. Such information is essential to evaluate fully the potential response of G. bulloides to ocean acidification and climate change. To investigate possible ecological interactions between G. bulloides and marine bacteria, 18S rRNA gene sequencing, fluorescence microscopy, 16S rRNA gene metabarcoding and transmission electron microscopy (TEM) were performed on individual specimens of G. bulloides (type IId) collected from two locations in the California Current. Intracellular DNA extracted from five G. bulloides specimens was subjected to 16S rRNA gene metabarcoding and, remarkably, 37–87 % of all 16S rRNA gene sequences recovered were assigned to operational taxonomic units (OTUs) from the picocyanobacterium Synechococcus. This finding was supported by TEM observations of intact Synechococcus cells in both the cytoplasm and vacuoles of G. bulloides. Their concentrations were up to 4 orders of magnitude greater inside the foraminifera than those reported for the California Current water column and approximately 5 % of the intracellular Synechococcus cells observed were undergoing cell division. This suggests that Synechococcus is an endobiont of G. bulloides type IId, which is the first report of a bacterial endobiont in the planktonic foraminifera. We consider the potential roles of Synechococcus and G. bulloides within the relationship and the need to determine how widespread the association is within the widely distributed G. bulloides morphospecies. The possible influence of Synechococcus respiration on G. bulloides shell geochemistry is also explored.
Highlights
Mutualistic associations between organisms in marine ecosystems can provide the partners involved with the capacity to adapt to environmental stresses such as energy or nutrient limitation as well as provide robustness under the challenges caused by climate change
G. bulloides specimen BUL34 is type IId and N. dutertrei specimen DUT55 is type Ic and it is the first time a ∼ 1000 bp fragment has been amplified for this genotype
Of greater present significance were the very many fluorescent, globular structures of approximately 1 μm diameter observed consistently within all of the G. bulloides cells analysed. Their small, regular size is consistent with the presence of intact intracellular bacteria residing within the foraminiferal cell (Fig. 2b)
Summary
Mutualistic associations between organisms in marine ecosystems can provide the partners involved with the capacity to adapt to environmental stresses such as energy or nutrient limitation as well as provide robustness under the challenges caused by climate change. The close association between photosynthetic microalgae and planktonic foraminifera supplies valuable fixed carbon and other benefits to the host and is a common feature of oligotrophic surface waters (Decelle et al, 2015). Since Murray first proposed a symbiotic role for these intracellular phototrophs in 1897 (Murray, 1897), many cytological and ultrastructural studies using light, fluorescence, and transmission electron microscopy have confirmed the presence of intracellular photosynthetic dinoflagellates or chrysophyte algae in a wide range of planktonic foraminifera (see Gastrich, 1987; Hemleben et al, 1989). Other experimental techniques focused on tracing radiolabelled C and N (Gastrich and Bartha, 1988), stable isotope analysis (Uhle et al, 1997, 1999), and microsensor studies of the chemical microenvironment (Jørgensen et al, 1985; Rink et al, 1998). Direct microscopic observations remain an important first step in assessing potential symbiotic associations
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