An ectobiont‐bearing foraminiferan, Bolivina pacifica, that inhabits microxic pore waters: cell‐biological and paleoceanographic insights

Abstract

SummaryThe presence of tests (shells) in foraminifera could be taken as an indicator that this protist taxon is unlikely to possess ectosymbionts. Here, however, we describe an association between Bolivina pacifica, a foraminiferan with a calcareous test, and a rodshaped microbe (bacterium or archaeon) that is directly associated with the pores of the foraminiferan's test. In addition to these putative ectosymbionts, B. pacifica has previously undescribed cytoplasmic plasma membrane invaginations (PMIs). These adaptations (i.e. PMIs, ectobionts), along with the clustering of mitochondria under the pores and at the cell periphery, suggest active exchange between the host and ectobiont. The B. pacifica specimens examined were collected from sediments overlain by oxygen-depleted bottom waters (0.7 mM) of the Santa Barbara Basin (California, USA). An ultrastructural comparison between B. pacifica from the Santa Barbara Basin and a congener (Bolivina cf. B. lanceolata) collected from well-oxygenated sediments (Florida Keys) suggests that PMIs, ectobionts and peripherally distributed mitochondria are all factors that promote inhabitation of microxic environments by B. pacifica. The calcitic d 13 C signatures of B. pacifica and of a co-occurring congener (B. argentea) that lacks ectobionts differ by > 1.5‰, raising the possibility that the presence of ectobionts can affect incorporation of paleoceanographic proxies.

Denitrification likely catalyzed by endobionts in an allogromiid foraminifer

“…Thus, our data suggests that denitrification in some species may be dominated by prokaryotic associates. Given that bacterial symbionts in benthic foraminiferal species from anoxic to micro-oxic habitats are not uncommon (Bernhard et al, 2000;Bernhard, 2003;Bernhard et al, 2010) and many or most of the foraminiferal species reported to denitrify (Piñ a-Ochoa et al, 2010) have not been examined for endo-and/or ectobionts, the role of prokaryotes in these associations deserves further study to resolve the enigma of foraminiferal denitrification. It is possible that other foraminiferal species, especially those lacking symbionts, may indeed perform complete denitrification but additional comparative studies using symbiont bearing and non-symbiont bearing species, as well as antibiotic treatments are required to shed more light on the ability of these eukaryotes to denitrify.…”

Test morphology as a function of behavioral strategies — Inferences from benthic foraminifera

“…Leutenegger and Hansen, 1979;Bernhard et al, 2010;Glock et al, 2012;Kuhnt et al, 2014). However, these investigations were conducted on a small number of different groups of benthic foraminifera, namely, mostly on Bolivina,…”

“…More recent interpretations of the function of pores in bolivinids (Bolivina spissa) suggest that they play a role in nitrate respiration (Høgslung, 2008;Glaud et al, 2009;Glock et al, 2012;Kuhnt et al, 2014) which makes it possible for the foraminifera to live in extreme environments with no or limited oxygen. Bernhard et al (2010) showed that pores (diameter 2.9-0,4 μm) of some bolivinid foraminifera (Bolivina pacifica) are directly associated with some ecosymbionts (bacteria and archaea) allowing active exchanges between the host and the ectobionts.…”

Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution

“…These include a wide range of metabolic relationships observed in shallow marine, primarily reducing environments, including endosymbiotic methanogens in ciliates to epibiotic hydrogen sulfide oxidizers on euglenids Ott, 1996;Epstein et al, 1998). The first observations of episymbiotic relationships between protists and prokaryotes in the deep sea were documented in cold seeps of Monterey Bay, CA, USA (Buck and Barry, 1998;Buck et al, 2000) and in the oxygen-depleted Santa Barbara Basin, CA, USA (Bernhard et al, 2000(Bernhard et al, , 2010. Both sites were at water depths greater than 500 m, and had high concentrations of mat-forming chemoautotrophic bacteria.…”

“…Hypotheses for the biological role(s) of rod-shaped epibionts of eukaryotic hosts usually involve commensalism, with the bacteria benefiting from metabolic byproducts secreted by the host Simpson et al, 1997;Leander and Keeling, 2004). It has also been hypothesized that the epibionts might be chemoautotrophic sulfur-or methane-oxidizers that form a mutualistic relationship with the host, whereby the host provides a substrate for the bacteria and the bacteria detoxify the immediate environment for the host (Bernhard, 2003;Bernhard et al, 2003Bernhard et al, , 2010. Under certain conditions, the epibiotic bacteria may serve as food for the host (Breglia et al, 2010).…”