skip to main content


Title: Environmental predictors of electroactive bacterioplankton in small boreal lakes
Abstract

Extracellular electron transfer (EET) by electroactive bacteria in anoxic soils and sediments is an intensively researched subject, but EET's function in planktonic ecology has been less considered. Following the discovery of an unexpectedly high prevalence of EET genes in a bog lake's bacterioplankton, we hypothesized that the redox capacities of dissolved organic matter (DOM) enrich for electroactive bacteria by mediating redox chemistry. We developed the bioinformatics pipeline FEET (Find EET) to identify and summarize predicted EET protein‐encoding genes from metagenomics data. We then applied FEET to 36 bog and thermokarst lakes and correlated gene occurrence with environmental data to test our predictions. Our results provide indirect evidence that DOM may participate in bacterioplankton EET. We found a similarly high prevalence of genes encoding putative EET proteins in most of these lakes, where oxidative EET strongly correlated with DOM. Numerous novel clusters of multiheme cytochromes that may enable EET were identified. Taxa previously not considered EET‐capable were found to carry EET genes. We propose that EET and DOM interactions are of ecologically important to bacterioplankton in small boreal lakes, and that EET, particularly by methylotrophs and anoxygenic phototrophs, should be further studied and incorporated into methane emission models of melting permafrost.

 
more » « less
Award ID(s):
2025982
NSF-PAR ID:
10401163
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
25
Issue:
3
ISSN:
1462-2912
Page Range / eLocation ID:
p. 705-720
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Microorganisms are strongly influenced by the bottom-up effects of resource supply. While many species respond to fluctuations in the concentration of resources, microbial diversity may also be affected by the heterogeneity of the resource pool, which often reflects a mixture of distinct molecules. To test this hypothesis, we examined resource–diversity relationships for bacterioplankton in a set of north temperate lakes that varied in their concentration and composition of dissolved organic matter (DOM), which is an important resource for heterotrophic bacteria. Using 16S rRNA transcript sequencing and ecosystem metabolomics, we documented strong relationships between bacterial alpha-diversity (richness and evenness) and the bulk concentration and the number of molecules in the DOM pool. Similarly, bacterial community beta-diversity was related to both DOM concentration and composition. However, in some lakes the relative abundance of resource generalists, which was inversely related to the DOM concentration, may have reduced the effect of DOM heterogeneity on community composition. Together, our results demonstrate the potential metabolic interactions between bacteria and organic matter and suggest that changes in organic matter composition may alter the structure and function of bacterial communities.

     
    more » « less
  2. Dubilier, Nicole (Ed.)
    ABSTRACT In the ocean surface layer and cell culture, the polyamine transport protein PotD of SAR11 bacteria is often one of the most abundant proteins detected. Polyamines are organic cations at seawater pH produced by all living organisms and are thought to be an important component of dissolved organic matter (DOM) produced in planktonic ecosystems. We hypothesized that SAR11 cells uptake and metabolize multiple polyamines and use them as sources of carbon and nitrogen. Metabolic footprinting and fingerprinting were used to measure the uptake of five polyamine compounds (putrescine, cadaverine, agmatine, norspermidine, and spermidine) in two SAR11 strains that represent the majority of SAR11 cells in the surface ocean environment, “ Candidatus Pelagibacter” strain HTCC7211 and “ Candidatus Pelagibacter ubique” strain HTCC1062. Both strains took up all five polyamines and concentrated them to micromolar or millimolar intracellular concentrations. Both strains could use most of the polyamines to meet their nitrogen requirements, but polyamines did not fully substitute for their requirements of glycine (or related compounds) or pyruvate (or related compounds). Our data suggest that potABCD transports all five polyamines and that spermidine synthase, speE, is reversible, catalyzing the breakdown of spermidine and norspermidine, in addition to its usual biosynthetic role. These findings provide support for the hypothesis that enzyme multifunctionality enables streamlined cells in planktonic ecosystems to increase the range of DOM compounds they metabolize. IMPORTANCE Genome streamlining in SAR11 bacterioplankton has resulted in a small repertoire of genes, yet paradoxically, they consume a substantial fraction of primary production in the oceans. Enzyme multifunctionality, referring to enzymes that are adapted to have broader substrate and catalytic range than canonically defined, is hypothesized to be an adaptation that increases the range of organic compounds metabolized by cells in environments where selection favors genome minimization. We provide experimental support for this hypothesis by demonstrating that SAR11 cells take up and metabolize multiple polyamine compounds and propose that a small set of multifunctional enzymes catalyze this metabolism. We report that polyamine uptake rates can exceed metabolic rates, resulting in both high intracellular concentrations of these nitrogen-rich compounds (in comparison to native polyamine levels) and an increase in cell size. 
    more » « less
  3. Abstract

    The dynamics of water and solutes were investigated in two northern bog ponds using sensor networks and discrete water samples. Embedded sensors monitored water level (S), precipitation (P), evaporation (E), water temperature (T) and specific conductivity (SC) in the peatlands and encircled ponds at 30 min time intervals from 2009 to 2015. Pond water chemistry was monitored seasonally from 2000 to 2020. Daily hydrographs and water budgets indicated that both bogs are ombrotrophic systems, perched above the local water table. Although the predominant flowpath for liquid water was precipitation → pond → peatland → underlying glacial deposits, evaporation accounted for 70% to 90% of water losses. High dissolved organic matter (DOM) in the ponds resulted from transient reversals of flowpath and from molecular diffusion across the peatland/pond interface (a tea bag effect). DOM of peatland origin dominated pond water chemistry, regulating the concentration of important metals, major nutrients and the acid–base status of both bog ponds. Elevated concentrations of Fe, Hg and MeHg in the ponds reflected ligand binding by DOM. The formation of DOM‐Fe‐PO4complexes likely accounted for >3‐fold higher P concentration relative to nearby clearwater lakes. Linear regression of dissolved organic carbon (DOC) against the anion deficit indicated that DOM contributed up to 6.6 mEq of strong acid per gramme carbon in pond waters. Winter maxima in the seasonal cycles of DOC, Ca, Mg, N, P, Hg and MeHg in both bog ponds were attributable, in large part, to salting out during ice formation. We conclude that multiple methods are needed to understand the dynamics of water and solutes in bog ecosystems.

     
    more » « less
  4. Abstract

    Global change is influencing production and respiration in ecosystems across the globe. Lakes in particular are changing in response to climatic variability and cultural eutrophication, resulting in changes in ecosystem metabolism. Although the primary drivers of production and respiration such as the availability of nutrients, light, and carbon are well known, heterogeneity in hydrologic setting (for example, hydrological connectivity, morphometry, and residence) across and within regions may lead to highly variable responses to the same drivers of change, complicating our efforts to predict these responses. We explored how differences in hydrologic setting among lakes influenced spatial and inter annual variability in ecosystem metabolism, using high-frequency oxygen sensor data from 11 lakes over 8 years. Trends in mean metabolic rates of lakes generally followed gradients of nutrient and carbon concentrations, which were lowest in seepage lakes, followed by drainage lakes, and higher in bog lakes. We found that while ecosystem respiration (ER) was consistently higher in wet years in all hydrologic settings, gross primary production (GPP) only increased in tandem in drainage lakes. However, interannual rates of ER and GPP were relatively stable in drainage lakes, in contrast to seepage and bog lakes which had coefficients of variation in metabolism between 22–32%. We explored how the geospatial context of lakes, including hydrologic residence time, watershed area to lake area, and landscape position influenced the sensitivity of individual lake responses to climatic variation. We propose a conceptual framework to help steer future investigations of how hydrologic setting mediates the response of metabolism to climatic variability.

     
    more » « less
  5. Abstract The Bay of Bengal receives nitrogen inputs from multiple sources and the potential role of nitrogen-metabolizing microbial communities in the surface water is not well understood. The nitrogen budget estimate shows a deficit of 4.7 ± 2.4 Tg N yr -1 , suggesting a significant role of dissolved organic nitrogen remineralization in fuelling ecosystem processes. Unravelling the process of remineralization leading to increasing concentrations of dissolved inorganic nitrogen (DIN) in coastal ecosystems such as in mangroves require a better understanding of the composition of functional resident bacterioplankton communities. Bacterioplankton communities were elucidated from eight stations along different estuaries spanning west to east of northeast coastal Bay of Bengal to understand the influence of DIN on shaping these communities. The eight stations were differentiated into ‘low’ and ‘high’ DIN stations based on DIN concentration, with five stations with High DIN concentration (>45 μ M) and three stations with Low DIN concentration (<40 μ M). The V3–V4 region of 16S rRNA was amplified and sequenced to elucidate resident bacterioplankton community structure from environmental DNA. Proteobacteria, Bacteroidetes, and Firmicutes were the dominant bacterioplankton phyla across all stations. Nitrogen-fixing groups such as Nitrospirae, Lentisphaerae, Chloroflexi, and Planctomycetes make up about 1% of the bacterioplankton communities. Abundances of Spirochaetes and Tenericutes showed a positive correlation with DIN. Pseudomonadales, Alteromonadales, and Desulfovibrionales were found to distinctly vary in abundance between Low and High DIN stations. Predicted metagenomic profiles from taxonomically derived community structures indicated bacterial nitrate-nitrite reductase to be negatively correlated with prevalent DIN concentration in High DIN stations but positively correlated in Low DIN stations. This trend was also consistent for genes encoding for nitrate/nitrite response regulators and transporter proteins. This indicates the need to delineate functional bacterioplankton community structures to better understand their role in influencing rates and fluxes of nitrogen within mangroves. 
    more » « less