Morphological Plasticity in a Sulfur-Oxidizing Marine Bacterium from the SUP05 Clade Enhances Dark Carbon Fixation

Abstract

Sulfur-oxidizing bacteria from the SUP05 clade are abundant in anoxic and oxygenated marine waters that appear to lack reduced sources of sulfur for cell growth. This raises questions about how these chemosynthetic bacteria survive across oxygen and sulfur gradients and how their mode of survival impacts the environment. Here, we use growth experiments, proteomics, and cryo-electron tomography to show that a SUP05 isolate, “Candidatus Thioglobus autotrophicus,” is amorphous in shape and several times larger and stores considerably more intracellular sulfur when it respires oxygen. We also show that these cells can use diverse sources of reduced organic and inorganic sulfur at submicromolar concentrations. Enhanced cell size, carbon content, and metabolic activity of the aerobic phenotype are likely facilitated by a stabilizing surface-layer (S-layer) and an uncharacterized form of FtsZ-less cell division that supports morphological plasticity. The additional sulfur storage provides an energy source that allows cells to continue metabolic activity when exogenous sulfur sources are not available. This metabolic flexibility leads to the production of more organic carbon in the ocean than is estimated based solely on their anaerobic phenotype. IMPORTANCE Identifying shifts in microbial metabolism across redox gradients will improve efforts to model marine oxygen minimum zone (OMZ) ecosystems. Here, we show that aerobic morphology and metabolism increase cell size, sulfur storage capacity, and carbon fixation rates in “Ca. Thioglobus autotrophicus,” a chemosynthetic bacterium from the SUP05 clade that crosses oxic-anoxic boundaries.

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

“…In some habitats, they will encounter sulfide. The sulfur cycle is generally coupled with the carbon cycle (46)(47)(48); however, it is still unclear how sulfide affects Synechococcus spp. and how they deal with it.…”

Facultative chemosynthesis in a deep-sea anemone from hydrothermal vents in the Pescadero Basin, Gulf of California

“…Like other SUP05 cells, those associated with the tentacles of O. pearseae were small (~500 nm in diameter; Shah et al 2019). Presumably these symbionts require both oxygen and sulfide near simultaneously, for example "Candidatus Thioglobus autotrophicus", a member of the SUP05 group, has an aerobic phenotype, and uses sulfide while respiring oxygen (Marshall and Morris 2013;Shah et al 2019). In this regard, it would be reasonable to house bacteria as close to the tissue surface as possible in order to accommodate gas exchange and meet symbiont metabolic demands.…”

“…Additionally, the epidermis in Anthozoa can function in nutrition (Fautin & Mariscal 1991), even more so than the gastrodermis, through direct uptake of dissolved organic compounds (Schlichter 1975(Schlichter , 1980, thus the positioning of nutritional bacteria in the epidermis may increase effective exchange of small molecules. Like other SUP05 cells, those associated with the tentacles of O. pearseae were small (~500 nm in diameter; Shah et al 2019). Presumably these symbionts require both oxygen and sulfide near simultaneously, for example "Candidatus Thioglobus autotrophicus", a member of the SUP05 group, has an aerobic phenotype, and uses sulfide while respiring oxygen (Marshall and Morris 2013;Shah et al 2019).…”

“…* > 70% support (using the Jukes Kantor model). Additional taxa were included according toPetersen et al 2012; Glaubitz et al 2013;Shah et al 2019. Inset. Shows SUP05 amplicons recovered from Ostiactis pearseae, surrounding seawater samples, and Bathymodiolus mussels from the Costa Rica margin Jaco Scar seep sites(SG, unpublished).…”

Quick microbial molecular phenotyping by differential shotgun proteomics

“…2 and 3. First, Shah et al (Shah et al, 2019) described the comparative proteomic analysis of a marine sulfur-oxidizing isolate, 'Candidatus Thioglobus autotrophicus', grown under oxic versus anoxic conditions with varying levels of sulfur availability. The authors analysed biological triplicates and identified peptides using a Q-Exactive HF tandem mass spectrometer following a 145-min reverse-phase gradient.…”