Starvation of the bacteria Vibrio atlanticus promotes lightning group-attacks on the dinoflagellate Alexandrium pacificum
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eLife Assessment
This important study convincingly shows that Vibrio bacteria act as predators of ecologically significant algae that contribute to harmful blooms in the lab, as well as in their natural habitat. While the data strongly suggest that starvation may induce predation, further work is needed to fully establish this link. Similarly, the evidence for a social component in the predation process remains incomplete. This study will be very impactful to those interested in the diversity of microbial predator-prey interactions and controlling toxic algal bloom, but the paper could be strengthened by more clearly showing the degree of replication, by better defining the terms used to describe the observed behaviour, and by providing better support for starvation and collective behaviour.
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Abstract
Abstract
Algae serve as a source of nutrients for bacteria in the marine environment. The interactions between algae and bacteria at the phycosphere interface are known to include mutualism, commensalism, competition or antagonism. Here, based on in situ observation and on an in vitro interaction study, we report on a novel form of starvation-induced hunting that the cells of selected Vibrio species exert on the dinoflagellate species. Results showed that Vibrio atlanticus was able to coordinate lightning group attacks then kill the dinoflagellate Alexandrium pacificum ACT03. Briefly, the observed coordinated mechanism of algal-killing consists of first, the ‘immobilization stage’ involving the secretion of algicidal metabolites that disrupt the flagella of the prey. The ‘attack stage’ resembles the ‘wolf-pack attack’ strategy, during which Vibrios surrounds algal cells at high density for a brief period without invading them. Finally, the ‘killing stage’ induces the lysis and degradation of the dinoflagellates. By using a combination of biochemical, proteomic, genetic and fluorescence microscopy approaches, we showed that this relationship is not related to the decomposition of algal organic matter, Vibrio quorum sensing pathways, to the toxicity of the algae or to the pathogenicity of the bacterium but is conditioned by nutrient stress, iron availability and link to the iron-vibrioferrin transport system of V. atlanticus. This is the first evidence of a new mechanism that could be involved in regulating Alexandrium spp. blooms and giving Vibrio a competitive advantage in obtaining nutrients from the environment.
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eLife Assessment
This important study convincingly shows that Vibrio bacteria act as predators of ecologically significant algae that contribute to harmful blooms in the lab, as well as in their natural habitat. While the data strongly suggest that starvation may induce predation, further work is needed to fully establish this link. Similarly, the evidence for a social component in the predation process remains incomplete. This study will be very impactful to those interested in the diversity of microbial predator-prey interactions and controlling toxic algal bloom, but the paper could be strengthened by more clearly showing the degree of replication, by better defining the terms used to describe the observed behaviour, and by providing better support for starvation and collective behaviour.
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Reviewer #1 (Public review):
Summary:
Rolland and colleagues investigated the interaction between Vibrio bacteria and Alexandrium algae. The authors found a correlation between the abundance of the two in the Thau Lagoon and observed in the laboratory that Vibrio grows to higher numbers in the presence of the algae than in monoculture. Time-lapse imaging of Alexandrium in coculture with Vibrio enabled the authors to observe Vibrio bacteria in proximity to the algae and subsequent algae death. The authors further determine the mechanism of the interaction between the two and point out similarities between the observed phenotypes and predator-prey behaviours across organisms.
Strengths:
The study combines field work with mechanistic studies in the laboratory and uses a wide array of techniques ranging from co-cultivation experiments to …
Reviewer #1 (Public review):
Summary:
Rolland and colleagues investigated the interaction between Vibrio bacteria and Alexandrium algae. The authors found a correlation between the abundance of the two in the Thau Lagoon and observed in the laboratory that Vibrio grows to higher numbers in the presence of the algae than in monoculture. Time-lapse imaging of Alexandrium in coculture with Vibrio enabled the authors to observe Vibrio bacteria in proximity to the algae and subsequent algae death. The authors further determine the mechanism of the interaction between the two and point out similarities between the observed phenotypes and predator-prey behaviours across organisms.
Strengths:
The study combines field work with mechanistic studies in the laboratory and uses a wide array of techniques ranging from co-cultivation experiments to genetic engineering, microscopy and proteomics. Further, the authors test multiple Vibrio and Alexandria species and claim a wide spread of the observed phenotypes.
Weaknesses:
In my view, the presentation of the data is in some cases not ideal. The phrasing of some conclusions (e.g., group-attacks and wolf-pack-hunting by the bacteria) is in my opinion too strong based on the herein provided data.
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Reviewer #2 (Public review):
Goal summary:
The authors sought to (i) demonstrate correlations between the dynamics of the dinoflagellate Alexandrium pacificum and the bacterim Vibrio atlanticus in natural populations, ii) demonstrate the occurrence of predation in laboratory experiments, iii) claim coordinated action by the predators in the predation process, iv) demonstrate that predation is induced by predator starvation, and v) test for effects of quorum sensing and iron-uptake genes on the predation process.
Strengths include:
(1) Data indicating correlated dynamics in a natural environment that increase the motivation for the study of in vitro interactions.
(2) Experimental design allowing clear inference of predation based on population counts of both prey and predators in addition to microscopy-based evidence.
(3) Supplementation …
Reviewer #2 (Public review):
Goal summary:
The authors sought to (i) demonstrate correlations between the dynamics of the dinoflagellate Alexandrium pacificum and the bacterim Vibrio atlanticus in natural populations, ii) demonstrate the occurrence of predation in laboratory experiments, iii) claim coordinated action by the predators in the predation process, iv) demonstrate that predation is induced by predator starvation, and v) test for effects of quorum sensing and iron-uptake genes on the predation process.
Strengths include:
(1) Data indicating correlated dynamics in a natural environment that increase the motivation for the study of in vitro interactions.
(2) Experimental design allowing clear inference of predation based on population counts of both prey and predators in addition to microscopy-based evidence.
(3) Supplementation of population-level data with molecular approaches to test hypotheses regarding possible involvement of quorum sensing and iron uptake in predation.
Weaknesses include:
(1) A lack of early, clear definitions for several important terms used in the paper, including 'predation', 'coordination' and 'coordinated action', 'group attack', and 'wolf-pack hunting', along with a corresponding lack of criteria for what evidence would warrant use of some of these labels. (For example, does mere simultaneity of attacks of an A. pacificum cell by many V. atlanticus cells constitute "coordination"? Or, as it seems to us, does coordination require some form of signalling between predator cells?)
(2) Absence of controls for cell density in the test for starvation effects on predatory behavior; unclear how the length of incubation affects the density of V. atlanticus cells.
(3) Lack of clarity in some of the methodological descriptions
Appraisal:
The authors convincingly achieve their aim of demonstrating that V. atlanticus can prey on A. pacificum, provide strongly suggestive evidence that such predation is induced by starvation, and clearly demonstrate that both iron availability and, correspondingly, the presence of genes involved in iron uptake, strongly influence the efficacy of predation. However, the evidence for starvation-induction of predation can be strengthened with cell-density controls; evidence for a social component to predation - positive interactions between attacking predators - is lacking.
Discussion of impact:
This paper will interest those interested in how microbial behaviour responds to environmental fluctuations, in particular predatory behaviour, but will do so more strongly if the evidence of starvation-induction of predation is strengthened. It will also interest those investigating bacteria-algae interactions and potential ecological controls of algal blooms. It has the potential to interest researchers of microbial cooperation, should the authors be able to provide any evidence of coordination between predator cells.
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