Broad distribution and high proportion of protein synthesis active marine bacteria revealed by click chemistry at the single cell level

Samo, Ty; Smriga, Steven; Malfatti, Francesca; Sherwood, Byron Pedler; Azam, Farooq

doi:10.3389/fmars.2014.00048

Cited by 48 publications

(93 citation statements)

References 76 publications

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“…Other environmental conditions not specifically addressed in our experiments, and potentially affecting this interaction will have to be assessed in future work, including nutrient concentrations, the combined effects of temperature and inorganic C availability (as affected by ocean acidification), and the effect of climate change on microbial community structure. Our results exemplify the concept that quantitative, functional analyses carried out on a single cell level can uncover cryptic interactions of potential importance at the ecosystem level, and NanoSIMS and other single-cell enabled microbial activity tools (Samo et al, 2014) are essential to collect such data.…”

Section: Discussionsupporting

confidence: 59%

Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

et al. 2016

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Quantifying the contribution of marine microorganisms to carbon and nitrogen cycles and their response to predicted ocean warming is one of the main challenges of microbial oceanography. Here we present a single-cell NanoSIMS isotope analysis to quantify C and N uptake by free-living and attached phytoplankton and heterotrophic bacteria, and their response to short-term experimental warming of 4°C. Elevated temperature increased total C fixation by over 50%, a small but significant fraction of which was transferred to heterotrophs within 12 h. Cell-to-cell attachment doubled the secondary C uptake by heterotrophic bacteria and increased secondary N incorporation by autotrophs by 68%. Warming also increased the abundance of phytoplankton with attached heterotrophs by 80%, and promoted C transfer from phytoplankton to bacteria by 17% and N transfer from bacteria to phytoplankton by 50%. Our results indicate that phytoplankton-bacteria attachment provides an ecological advantage for nutrient incorporation, suggesting a mutualistic relationship that appears to be enhanced by temperature increases.

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Section: Discussionsupporting

confidence: 59%

Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

et al. 2016

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“…This hetereogeneity is commonly averaged out in bulk sampling approaches and seldom appreciated in marine microbial ecology. Intriguingly, long-tailed distribution curves also characterize single-cell activity rates in coastal seawater (40,41), suggesting a relationship between the uptake heterogeneity resulting from hotspots and skewed rates in standing bacterial stocks, which may extend to the level of individual phylotypes.…”

Section: Significancementioning

confidence: 99%

Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria

Smriga

Fernández

Mitchell

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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215

213

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The microenvironment surrounding individual phytoplankton cells is often rich in dissolved organic matter (DOM), which can attract bacteria by chemotaxis. These "phycospheres" may be prominent sources of resource heterogeneity in the ocean, affecting the growth of bacterial populations and the fate of DOM. However, these effects remain poorly quantified due to a lack of quantitative ecological frameworks. Here, we used video microscopy to dissect with unprecedented resolution the chemotactic accumulation of marine bacteria around individual Chaetoceros affinis diatoms undergoing lysis. The observed spatiotemporal distribution of bacteria was used in a resource utilization model to map the conditions under which competition between different bacterial groups favors chemotaxis. The model predicts that chemotactic, copiotrophic populations outcompete nonmotile, oligotrophic populations during diatom blooms and bloom collapse conditions, resulting in an increase in the ratio of motile to nonmotile cells and in the succession of populations. Partitioning of DOM between the two populations is strongly dependent on the overall concentration of bacteria and the diffusivity of different DOM substances, and within each population, the growth benefit from phycospheres is experienced by only a small fraction of cells. By informing a DOM utilization model with highly resolved behavioral data, the hybrid approach used here represents a new path toward the elusive goal of predicting the consequences of microscale interactions in the ocean.bacteria-phytoplankton interactions | motility | competition | microbial loop | dissolved organic matter

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“…archaea and bacteria within environmental samples (9,14). BONCAT depends on the addition of a bioorthogonal (noninteracting with cellular functionalities) synthetic (noncanonical) amino acid to a sample.…”

Section: Significancementioning

confidence: 99%

“…In a proof-of-principle investigation, BONCAT was applied to environmental samples and found to be generally applicable to uncultured archaea and bacteria (9,14). BONCAT has been demonstrated to correlate well with other, independent proxies of cellular growth, i.e., the incorporation of isotopically labeled compounds as detected by nanoscale SIMS, 15 NH 4 + (9), and MAR, [ 35 S]Met (14). In addition, a protocol for the concomitant taxonomic identification of translationally active cells via rRNA-targeted FISH (i.e., BONCAT-FISH) was recently developed (9) (Fig.…”

Section: Significancementioning

confidence: 99%

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Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

Hatzenpichler

Connon

Goudeau

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

175

209

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To understand the biogeochemical roles of microorganisms in the environment, it is important to determine when and under which conditions they are metabolically active. Bioorthogonal noncanonical amino acid tagging (BONCAT) can reveal active cells by tracking the incorporation of synthetic amino acids into newly synthesized proteins. The phylogenetic identity of translationally active cells can be determined by combining BONCAT with rRNAtargeted fluorescence in situ hybridization (BONCAT-FISH). In theory, BONCAT-labeled cells could be isolated with fluorescenceactivated cell sorting (BONCAT-FACS) for subsequent genetic analyses. Here, in the first application, to our knowledge, of BONCAT-FISH and BONCAT-FACS within an environmental context, we probe the translational activity of microbial consortia catalyzing the anaerobic oxidation of methane (AOM), a dominant sink of methane in the ocean. These consortia, which typically are composed of anaerobic methane-oxidizing archaea (ANME) and sulfatereducing bacteria, have been difficult to study due to their slow in situ growth rates, and fundamental questions remain about their ecology and diversity of interactions occurring between ANME and associated partners. Our activity-correlated analyses of >16,400 microbial aggregates provide the first evidence, to our knowledge, that AOM consortia affiliated with all five major ANME clades are concurrently active under controlled conditions. Surprisingly, sorting of individual BONCAT-labeled consortia followed by whole-genome amplification and 16S rRNA gene sequencing revealed previously unrecognized interactions of ANME with members of the poorly understood phylum Verrucomicrobia. This finding, together with our observation that ANME-associated Verrucomicrobia are found in a variety of geographically distinct methane seep environments, suggests a broader range of symbiotic relationships within AOM consortia than previously thought.activity-based cell sorting | BONCAT | click chemistry | ecophysiology | single-cell microbiology

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Broad distribution and high proportion of protein synthesis active marine bacteria revealed by click chemistry at the single cell level

Cited by 48 publications

References 76 publications

Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria

Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

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