skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.
Attention:The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 7:00 AM ET to 7:30 AM ET on Friday, April 24 due to maintenance. We apologize for the inconvenience.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


  • NSF Public Access
  • Search Results
  • Diversity in the utilization of different molecular classes of dissolved organic matter by heterotrophic marine bacteria
Title: Diversity in the utilization of different molecular classes of dissolved organic matter by heterotrophic marine bacteria
ABSTRACT Heterotrophic marine bacteria utilize and recycle dissolved organic matter (DOM), impacting biogeochemical cycles. It is currently unclear to what extent distinct DOM components can be used by different heterotrophic clades. Here, we ask how a natural microbial community from the Eastern Mediterranean Sea (EMS) responds to different molecular classes of DOM (peptides, amino acids, amino sugars, disaccharides, monosaccharides, and organic acids) comprising much of the biomass of living organisms. Bulk bacterial activity increased after 24 h for all treatments relative to the control, while glucose and ATP uptake decreased or remained unchanged. Moreover, while the per-cell uptake rate of glucose and ATP decreased, that of Leucin significantly increased for amino acids, reflecting their importance as common metabolic currencies in the marine environment.Pseudoalteromonadaceaedominated the peptides treatment, while differentVibrionaceaestrains became dominant in response to amino acids and amino sugars.Marinomonadaceaegrew well on organic acids, andAlteromonadaseaeon disaccharides. A comparison with a recent laboratory-based study reveals similar peptide preferences forPseudoalteromonadaceae, whileAlteromonadaceae, for example, grew well in the lab on many substrates but dominated in seawater samples only when disaccharides were added. We further demonstrate a potential correlation between the genetic capacity for degrading amino sugars and the dominance of specific clades in these treatments. These results highlight the diversity in DOM utilization among heterotrophic bacteria and complexities in the response of natural communities. IMPORTANCEA major goal of microbial ecology is to predict the dynamics of natural communities based on the identity of the organisms, their physiological traits, and their genomes. Our results show that several clades of heterotrophic bacteria each grow in response to one or more specific classes of organic matter. For some clades, but not others, growth in a complex community is similar to that of isolated strains in laboratory monoculture. Additionally, by measuring how the entire community responds to various classes of organic matter, we show that these results are ecologically relevant, and propose that some of these resources are utilized through common uptake pathways. Tracing the path between different resources to the specific microbes that utilize them, and identifying commonalities and differences between different natural communities and between them and lab cultures, is an important step toward understanding microbial community dynamics and predicting how communities will respond to perturbations.  more » « less
Award ID(s):
2246707
PAR ID:
10537037
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Editor(s):
Biddle, Jennifer F
Publisher / Repository:
ASM
Date Published:
Journal Name:
Applied and Environmental Microbiology
Volume:
90
Issue:
7
ISSN:
0099-2240
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ; ; ; ; et al (, mSystems)
    Meyer, Julie L (Ed.)
    High molecular weight (HMW; >1 kDa) carbohydrates are a major component of dissolved organic matter (DOM) released by benthic primary producers. Despite shifts from coral to algae dominance on many reefs, little is known about the effects of exuded carbohydrates on bacterioplankton communities in reef waters. We compared the monosaccharide composition of HMW carbohydrates exuded by hard corals and brown macroalgae and investigated the response of the bacterioplankton community of an algae-dominated Caribbean reef to the respective HMW fractions. HMW coral exudates were compositionally distinct from the ambient, algae-dominated reef waters and similar to coral mucus (high in arabinose). They further selected for opportunistic bacterioplankton taxa commonly associated with coral stress (i.e.,Rhodobacteraceae,Phycisphaeraceae,Vibrionaceae, andFlavobacteriales) and significantly increased the predicted energy-, amino acid-, and carbohydrate-metabolism by 28%, 44%, and 111%, respectively. In contrast, HMW carbohydrates exuded by algae were similar to those in algae tissue extracts and reef water (high in fucose) and did not significantly alter the composition and predicted metabolism of the bacterioplankton community. These results confirm earlier findings of coral exudates supporting efficient trophic transfer, while algae exudates may have stimulated microbial respiration instead of biomass production, thereby supporting the microbialization of reefs. In contrast to previous studies, HMW coral and not algal exudates selected for opportunistic microbes, suggesting that a shift in the prevalent DOM composition and not the exudate type (i.e., coral vs algae)per se, may induce the rise of opportunistic microbial taxa. IMPORTANCEDissolved organic matter (DOM) released by benthic primary producers fuels coral reef food webs. Anthropogenic stressors cause shifts from coral to algae dominance on many reefs, and resulting alterations in the DOM pool can promote opportunistic microbes and potential coral pathogens in reef water. To better understand these DOM-induced effects on bacterioplankton communities, we compared the carbohydrate composition of coral- and macroalgae-DOM and analyzed the response of bacterioplankton from an algae-dominated reef to these DOM types. In line with the proposed microbialization of reefs, coral-DOM was efficiently utilized, promoting energy transfer to higher trophic levels, whereas macroalgae-DOM likely stimulated microbial respiration over biomass production. Contrary to earlier findings, coral- and not algal-DOM selected for opportunistic microbial taxa, indicating that a change in the prevalent DOM composition, and not DOM type, may promote the rise of opportunistic microbes. Presented results may also apply to other coastal marine ecosystems undergoing benthic community shifts. 
    more » « less
  2. ; ; ; ; ; ; ; ; ; ; et al (, ISME Communications)
    Abstract Dinitrogen (N₂) fixation by diazotrophs supports ocean productivity. Diazotrophs include photoautotrophic cyanobacteria, non-cyanobacterial diazotrophs (NCDs) and the recently discovered N2-fixing haptophyte. While NCDs are ubiquitous in the ocean, their ecology and metabolism remain largely unknown. Unlike cyanobacterial diazotrophs and the haptophyte, NCDs are primarily heterotrophic and depend on dissolved organic matter (DOM) for carbon and energy. However, conventional DOM amendment incubations do not allow discerning how different diazotrophs use DOM molecules, limiting our knowledge on DOM-diazotroph interactions. To identify diazotrophs using DOM, we amended North Pacific microbial communities with 13C-labeled DOM from phytoplankton cultures that was molecularly characterized, revealing the dominance of nitrogen-rich compounds. After DOM additions, we observed a community shift from cyanobacterial diazotrophs like Crocosphaera and Trichodesmium to NCDs at stations where the N2-fixing haptophyte abundance was relatively low. Through DNA stable isotope probing and gene sequencing, we identified diverse diazotrophs capable of taking up DOM. Our findings highlight unexpected DOM uptake by the haptophyte’s nitroplast, changes in community structure, and previously unrecognized osmotrophic behavior in NCDs, shaped by local biogeochemical conditions. 
    more » « less
  3. ; ; ; ; ; ; (, The ISME Journal)
    null (Ed.)
    Abstract The communities of bacteria that assemble around marine microphytoplankton are predictably dominated by Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. Yet whether this consistent ecological pattern reflects the result of resource-based niche partitioning or resource competition requires better knowledge of the metabolites linking microbial autotrophs and heterotrophs in the surface ocean. We characterized molecules targeted for uptake by three heterotrophic bacteria individually co-cultured with a marine diatom using two strategies that vetted the exometabolite pool for biological relevance by means of bacterial activity assays: expression of diagnostic genes and net drawdown of exometabolites, the latter detected with mass spectrometry and nuclear magnetic resonance using novel sample preparation approaches. Of the more than 36 organic molecules with evidence of bacterial uptake, 53% contained nitrogen (including nucleosides and amino acids), 11% were organic sulfur compounds (including dihydroxypropanesulfonate and dimethysulfoniopropionate), and 28% were components of polysaccharides (including chrysolaminarin, chitin, and alginate). Overlap in phytoplankton-derived metabolite use by bacteria in the absence of competition was low, and only guanosine, proline, and N -acetyl- d -glucosamine were predicted to be used by all three. Exometabolite uptake pattern points to a key role for ecological resource partitioning in the assembly marine bacterial communities transforming recent photosynthate. 
    more » « less
  4. ; ; ; (, Ecology Letters)
    ABSTRACT Benthic–pelagic coupling, the reciprocal exchange of materials between benthic and pelagic habitats, has traditionally emphasised pelagic influences on benthic systems. Yet, the role of benthic biological processes in shaping pelagic microbial dynamics remains underexplored. We investigated how surfgrass and mussels regulate nitrogen and dissolved organic matter (DOM) cycling and their cascading effects on heterotrophic bacteria in Oregon tide pools. We quantified biogeochemical fluxes and bacterial responses before and after foundation species removal during contrasting upwelling regimes. Mussel‐dominated pools released high concentrations of ammonium and nitrate, while surfgrass pools transformed DOM that fueled bacterial growth; upwelling intensified these benthic–pelagic linkages. Removing foundation species dampened nutrient release in mussel pools and reduced DOM‐fueled bacterial growth in surfgrass pools, ultimately decoupling benthic productivity from pelagic microbial growth. Our results demonstrate the critical role of foundation species to pelagic microbial processes and underscore the vulnerability of coastal microbial dynamics to their global decline. 
    more » « less
  5. ; ; ; (, Microbiology Spectrum)
    Steven, Blaire (Ed.)
    ABSTRACT Microbes are essential for the functioning of all ecosystems, and as global warming and anthropogenic pollution threaten ecosystems, it is critical to understand how microbes respond to these changes. We investigated the climate response ofSphingomonas, a widespread gram-negative bacterial genus, during an 18-month microbial community reciprocal transplant experiment across a Southern California climate gradient. We hypothesized that after 18 months, the transplantedSphingomonasclade and functional composition would correspond with site conditions and reflect theSphingomonascomposition of native communities. We extractedSphingomonassequences from metagenomic data across the gradient and assessed their clade and functional composition. Representatives of at least 12 majorSphingomonasclades were found at varying relative abundances along the climate gradient, and transplantedSphingomonasclade composition shifted after 18 months. Site had a significant effect (PERMANOVA;P< 0.001) on the distribution of bothSphingomonasfunctional (R2= 0.465) and clade composition (R2= 0.400), suggesting thatSphingomonascomposition depends on climate parameters. Additionally, for bothSphingomonasclade and functional composition, ordinations revealed that the transplanted communities shifted closer to the nativeSphingomonascomposition of the grassland site compared with the site they were transplanted into. Overall, our results indicate that climate and substrate collectively determineSphingomonasclade and functional composition.IMPORTANCESphingomonasis the most abundant gram-negative bacterial genus in litter-degrading microbial communities of desert, grassland, shrubland, and forest ecosystems in Southern California. We aimed to determine whetherSphingomonasresponds to climate change in the same way as gram-positive bacteria and whole bacterial communities in these ecosystems. WithinSphingomonas, both clade composition and functional genes shifted in response to climate and litter chemistry, supporting the idea that bacteria respond similarly to climate at different scales of genetic variation. This understanding of how microbes respond to perturbation across scales may aid in future predictions of microbial responses to climate change. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Text Encoded Conversion
  • XML
  • Save / Share this Record
  • Send to Email