Cytologic and Genetic Characteristics of Endobiotic Bacteria and Kleptoplasts of Virgulinella fragilis (Foraminifera)

Abstract

The benthic foraminifer Virgulinella fragilis Grindell and Collen 1976 has multiple putative symbioses with both bacterial and kleptoplast endobionts, possibly aiding its survival in environments from dysoxia (5-45 μmol-O2 /L) to microxia (0-5 μmol-O2 /L) and in the dark. To clarify the origin and function of V. fragilis endobionts, we used genetic analyses and transmission electron microscope observations. Virgulinella fragilis retained δ-proteobacteria concentrated at its cell periphery just beneath the cell membranes. Unlike another foraminifer Stainforthia spp., which retains many bacterial species, V. fragilis has a less variable bacterial community. This suggests that V. fragilis maintains a specific intracellular bacterial flora. Unlike the endobiotic bacteria, V. fragilis klepto-plasts originated from various diatom species and are found in the interior cytoplasm. We found evidence of both retention and digestion of kleptoplasts, and of fragmentation of the kleptoplastid outer membrane that likely facilitates transport of kleptoplastid products to the host. Accumulations of mitochondria were observed encircling endobiotic bacteria. It is likely that the bacteria use host organic material for carbon oxidation. The mitochondria may use oxygen available around the δ-proteobacteria and synthesize adenosine triphosphate, perhaps for sulfide oxidation.

Compound‐specific isotope analysis of benthic foraminifer amino acids suggests microhabitat variability in rocky‐shore environments

“…() and Tsuchiya et al. (). The TEM observation was carried out using a TECNAI G 2 20 transmission electron microscope (FEI, Hillsboro, OR, USA) at an acceleration voltage of 120 kV.…”

“…Detailed methods involved in individual sorting, PCR amplification, cloning, and sequencing have been described by Tsuchiya et al. (, ). We searched for the most similar sequences using the Basic Local Alignment Search Tool (BLAST) with homology search option (National Center for Biotechnology Information, National Institutes of Health, Bethesda, MD, USA).…”

Changes in ultrastructural features of the foraminifera Ammonia spp. in response to anoxic conditions: Field and laboratory observations

“…(phylotype 6 and phylotype unknown) may be a host to various species of intracellular bacteria, and that the bacterial assemblages comprising the foraminiferal microbiome may change in time and space. Various endobionts have been described for other foraminiferal species that inhabit anoxic sediments (e.g., Bernhard, 2003;Bernhard et al, 2012;Tsuchiya et al, 2015;Bernhard et al, 2017). Therefore, the presence of bacterial endobionts in foraminifera coming from anoxic sediments seems relatively widespread.…”

“…Presence of potential endosymbionts involved in denitrification or other biogeochemical functions, enabling foraminifera to survive anoxia, can be detected and visualized. Many species of benthic foraminifera, which inhabit low-oxygen environments, seem to possess various potential endosymbionts (e.g., Bernhard, 1993;Bernhard, 1996;Bernhard, 2003;Bernhard et al, 2012;Tsuchiya et al, 2015;Bernhard et al, 2017). Extensive peroxisomes complexed with endoplasmic reticulum, which are atypical in foraminifera from aerated habitats, have also been linked to foraminiferal survival in low-oxygen and chemocline sediments (e.g., Nyholm and Nyholm 1975, Bernhard, 1996, Bernhard and Bowser, 2008.…”

Kleptoplastidic benthic foraminifera from aphotic habitats: insights into assimilation of inorganic C, N and S studied with sub‐cellular resolution

“…Among these adaptations, some species have the ability to ingest and maintain intact chloroplasts (kleptoplasts) in their cytosol from days to many months (Correia and Lee, ; Grzymski et al ., ). This process is called kleptoplasty (Clark et al ., ) and has been observed in multiple intertidal to deep‐sea foraminifera (Lopez, ; Lee et al ., ; Cedhagen, ; Bernhard and Bowser, ; Correia and Lee, ; , ; Bernhard, ; Goldstein et al ., ; Pillet et al ., ; Tsuchiya et al ., ; Goldstein and Richardson, ; Jauffrais et al ., ).…”