Decrypting the sulfur cycle in oceanic oxygen minimum zones

Crowe, Sean A.; Cox, Raymond P.; Jones, Craig; Fowle, David A.; Santibañez-Bustos, J. F.; Ulloa, Osvaldo; Canfield, Donald E.

doi:10.1038/s41396-018-0149-2

Cited by 15 publications

(23 citation statements)

References 32 publications

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“…The highest specific growth rates measured under anoxic growth conditions were in media with 1 μM sulfide added, whereas sulfide concentrations of >1 μM inhibited growth. Recent evidence of high-affinity sulfide uptake by SUP05 in anoxic marine waters indicates that there is a cryptic marine sulfur cycle operating at below-detection (nanomolar) substrate concentrations (20). Here, we show that sources of reduced sulfur other than sulfide, including organic sulfur, could support a cryptic sulfur cycle in oxygenated seawater with concentrations as low as 10 nM.…”

Section: Resultsmentioning

confidence: 99%

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

Shah

Zhao

Lundeen

et al. 2019

mBio

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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.

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Section: Resultsmentioning

confidence: 99%

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

Shah

Zhao

Lundeen

et al. 2019

mBio

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“…The affinity of SUP05 bacteria for sulfide is higher than reported for any other bacterium or substrate (Crowe et al ., 2018 ), demanding a re‐evaluation of the existing definition of euxinia. Currently, the sulfide concentration threshold to distinguish non‐sulfidic from euxinic conditions commonly falls in the range of 0.5–1 μM.…”

Section: Sulfur‐oxidizing Bacteriamentioning

confidence: 99%

“…This threshold is similar to the in vitro Michaelis–Menten half‐saturation constant ( K m ) of 2 μM of purified high‐affinity Sqr proteins (Schutz et al ., 1997 ; Brito et al ., 2009 ) and the K m found for phototrophic SOB (> 0.8 μM; Van Gemerden, 1984 ). However, the estimated K m of SUP05 bacteria is much lower (25–340 nM; Crowe et al ., 2018 ). The most widely used method for determining sulfide concentrations has a sulfide detection limit of 0.1 μM (Cline, 1969 ; Jørgensen et al ., 1991 ; Zopfi et al ., 2001 ), hence falling within this estimated range.…”

Section: Sulfur‐oxidizing Bacteriamentioning

confidence: 99%

The bacterial sulfur cycle in expanding dysoxic and euxinic marine waters

Vliet

Meijenfeldt

Dutilh

et al. 2020

Environmental Microbiology

165

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Dysoxic marine waters (DMW, < 1 μM oxygen) are currently expanding in volume in the oceans, which has biogeochemical, ecological and societal consequences on a global scale. In these environments, distinct bacteria drive an active sulfur cycle, which has only recently been recognized for open-ocean DMW. This review summarizes the current knowledge on these sulfur-cycling bacteria. Critical bottlenecks and questions for future research are specifically addressed. Sulfate-reducing bacteria (SRB) are core members of DMW. However, their roles are not entirely clear, and they remain largely uncultured. We found support for their remarkable diversity and taxonomic novelty by mining metagenome-assembled genomes from the Black Sea as model ecosystem. We highlight recent insights into the metabolism of key sulfur-oxidizing SUP05 and Sulfurimonas bacteria, and discuss the probable involvement of uncultivated SAR324 and BS-GSO2 bacteria in sulfur oxidation. Uncultivated Marinimicrobia bacteria with a presumed organoheterotrophic metabolism are abundant in DMW. Like SRB, they may use specific molybdoenzymes to conserve energy from the oxidation, reduction or disproportionation of sulfur cycle intermediates such as S 0 and thiosulfate, produced from the oxidation of sulfide. We expect that tailored sampling methods and a renewed focus on cultivation will yield deeper insight into sulfur-cycling bacteria in DMW.

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“…The ability of SUP05 to store intracellular sulfur (Callbeck et al 2018; Shah et al 2019), combined with its affinity for low‐sulfide concentrations, could explain how they are able to persist throughout the spring–summer anoxic period in the ETSP region (Léniz et al 2017) (Fig. 2C), and even when dissolved sulfide is absent (Crowe et al 2018).…”

Section: Termination Of Sulfidic Events By a Succession Of Sulfide‐oxidizing Bacteriamentioning

confidence: 99%

Sulfur cycling in oceanic oxygen minimum zones

Callbeck

Canfield

Kuypers

et al. 2021

Limnology & Oceanography

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The sulfur cycle is an important, although understudied facet of today's modern oxygen minimum zones (OMZs). Sulfur cycling is most active in highly productive coastal OMZs where sulfide-rich sediments interact with the overlying water column, forming a tightly coupled benthic-pelagic sulfur cycle. In such productive coastal systems, highly eutrophic and anoxic conditions can result in the benthic release of sulfide leading to an intensification of OMZ-shelf biogeochemistry. Active blooms involving a succession of sulfide-oxidizing bacteria detoxify sulfide and reduce nitrate to N 2 , while generating nitrite and ammonium that augment anammox and nitrification. Furthermore, the abiotic interactions of sulfide with trace metals may have the potential to moderate nitrous oxide emissions. While sulfide/sulfur accumulation events were previously considered to be rare, new evidence indicates that events can develop in OMZ shelf waters over prolonged periods of anoxia. The prevalence of these events has ramifications for nitrogen loss and greenhouse gas emissions, including other linked cycles involving carbon and phosphorous. Sulfur-based metabolisms and activity also extend into the offshore OMZ as a result of particle microniches and lateral transport processes. Moreover, OMZ waters ubiquitously host a community of organosulfur-based heterotrophs that ostensibly moderate the turnover of organic sulfur, offering an exciting avenue for future research. Our synthesis highlights the widespread distribution and multifaceted nature of the sulfur cycle in oceanic OMZs.

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Decrypting the sulfur cycle in oceanic oxygen minimum zones

Cited by 15 publications

References 32 publications

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

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

The bacterial sulfur cycle in expanding dysoxic and euxinic marine waters

Sulfur cycling in oceanic oxygen minimum zones

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