Dynamic metabolic exchange governs a marine algal-bacterial interaction
- Harvard Medical School, United States
- Sungkyunkwan University, United States
- Leibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Germany
- Broad Institute, United States
- Dana-Farber Cancer Institute, United States
- The Hebrew University of Jerusalem, Israel
Abstract
Emiliania huxleyi is a model coccolithophore micro-alga that generates vast blooms in the ocean. Bacteria are not considered among the major factors influencing coccolithophore physiology. Here we show through a laboratory model system that the bacterium Phaeobacter inhibens, a well-studied member of the Roseobacter group, intimately interacts with E. huxleyi. While attached to the algal cell, bacteria initially promote algal growth but ultimately kill their algal host. Both algal growth enhancement and algal death are driven by the bacterially-produced phytohormone indole-3-acetic acid. Bacterial production of indole-3-acetic acid and attachment to algae are significantly increased by tryptophan, which is exuded from the algal cell. Algal death triggered by bacteria involves activation of pathways unique to oxidative stress response and programmed cell death. Our observations suggest that bacteria greatly influence the physiology and metabolism of E. huxleyi. Coccolithophore-bacteria interactions should be further studied in the environment to determine whether they impact micro-algal population dynamics on a global scale.
Data availability
-
Dynamic Metabolic Exchange Governs a Marine Algal-Bacterial InteractionPublicly available at the NCBI Sequence Read Archive (SRA accession: SRP075256).
Article and author information
Author details
Funding
European Molecular Biology Organization (LTF 649-2012)
- Einat Segev
Human Frontier Science Program (LT000061/2013-L)
- Einat Segev
DFG Transregio TRR-51 Roseobacter
- Jörn Petersen
PCMM
- Natasha Barteneva
National Institutes of Health (RR023459)
- Natasha Barteneva
National Institutes of Health (GM086258)
- Jon Clardy
National Institutes of Health (GM58213)
- Roberto Kolter
National Institutes of Health (GM82137)
- Roberto Kolter
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2016, Segev et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 7,960
- views
-
- 1,706
- downloads
-
- 217
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Dynamic metabolic exchange governs a marine algal-bacterial interaction
eLife 5:e17473.
https://doi.org/10.7554/eLife.17473
Further reading
-
- Ecology
- Neuroscience
Prey must balance predator avoidance with feeding, a central dilemma in prey refuge theory. Additionally, prey must assess predatory imminence—how close threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes: pre-encounter, post-encounter, and circa-strike, corresponding to increasing levels of threat—–suspecting, detecting, and contacting a predator. Although predatory risk often varies in spatial distribution and imminence, how these factors intersect to influence defensive behaviors is poorly understood. Integrating these factors into a naturalistic environment enables comprehensive analysis of multiple defense modes in consistent conditions. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. In a foraging environment comprised of a food-rich, high-risk patch and a food-poor, low-risk refuge, C. elegans innately exhibits circa-strike behaviors. With experience, it learns post- and pre-encounter behaviors that proactively anticipate threats. These defense modes intensify with predator lethality, with only life-threatening predators capable of eliciting all three modes. SEB-3 receptors and NLP-49 peptides, key stress regulators, vary in their impact and interdependence across defense modes. Overall, our model system reveals fine-grained insights into how stress-related signaling regulates defensive behaviors.
-
- Ecology
Understanding the relationships between biodiversity and ecosystem functioning stands as a cornerstone in ecological research. Extensive evidence now underscores the profound impact of species loss on the stability and dynamics of ecosystem functions. However, it remains unclear whether the loss of genetic diversity within key species yields similar consequences. Here, we delve into the intricate relationship between species diversity, genetic diversity, and ecosystem functions across three trophic levels – primary producers, primary consumers, and secondary consumers – in natural aquatic ecosystems. Our investigation involves estimating species diversity and genome-wide diversity – gauged within three pivotal species – within each trophic level, evaluating seven key ecosystem functions, and analyzing the magnitude of the relationships between biodiversity and ecosystem functions (BEFs). We found that, overall, the absolute effect size of genetic diversity on ecosystem functions mirrors that of species diversity in natural ecosystems. We nonetheless unveil a striking dichotomy: while genetic diversity was positively correlated with various ecosystem functions, species diversity displays a negative correlation with these functions. These intriguing antagonist effects of species and genetic diversity persist across the three trophic levels (underscoring its systemic nature), but were apparent only when BEFs were assessed within trophic levels rather than across them. This study reveals the complexity of predicting the consequences of genetic and species diversity loss under natural conditions, and emphasizes the need for further mechanistic models integrating these two facets of biodiversity.
