Strong effects of amoebae grazing on the biomass and genetic structure of a <i>Microcystis</i> bloom (Cyanobacteria)

Wichelen, Jeroen Van; Gremberghe, Ineke van; Vanormelingen, Pieter; Debeer, Ann-Eline; Leporcq, Bruno; Menzel, Diana; Codd, Geoffrey A.; Descy, Jean-Pierre; Vyverman, Wim

doi:10.1111/j.1462-2920.2010.02249.x

Cited by 55 publications

(33 citation statements)

References 91 publications

(101 reference statements)

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“…Rotifera, Cladocera and copepods were the most stable taxa, followed by protozoa, and the stability of phytoplankton taxa was the lowest. Protozoa prey on phytoplankton species, whereas both protozoa and phytoplankton are consumed by Rotifera, Cladocera and copepods [48,49]. Thus, the temporal stability of these taxa was consistent with their trophic levels in aquatic ecosystems: plankton taxa at higher trophic levels would be more stable.…”

Section: Discussionmentioning

confidence: 73%

Plankton Community Stability and Its Relationship with Phytoplankton Species Richness in Lake Nansihu, China

Zhang

Zhao

et al. 2016

Water

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Abstract:The relationship between biodiversity and ecosystem functioning is a central issue in ecology. The insurance hypothesis suggests that biodiversity could improve community productivity and reduce the temporal variability of main ecosystem processes. In the present study, we used a plankton community that was investigated from 2011 to 2014 in Lake Nansihu to test this hypothesis and explore the mechanisms involved. As a result, 138 phytoplankton and 76 zooplankton species were identified in the lake, and their biomasses showed apparent seasonal variations. The average temporal stability index of zooplankton taxa was significantly higher than that of phytoplankton. Complex relationships were observed between the species richness and temporal stability of different phytoplankton taxa: a unimodal relationship for both Cyanophyta and Bacillariophyta; a strong concave relationship for Euglenophyta; and no apparent relationship for both Chlorophyta and total phytoplankton. These relationships were primarily controlled by the portfolio effect; while the effects of overyielding and species asynchrony were relatively weak. Phytoplankton species richness had a significant positive influence on the temporal stability indices of protozoa, Rotifera and total zooplankton, while its influence on Cladocera and copepods was not significant. The dominant mechanisms were found to be 'trophic overyielding' and a weak 'trophic portfolio effect'; however, 'trophic species asynchrony' played a minor role. These results demonstrated that the effects of diversity on community stability can be complex in natural ecosystems. In addition, the diversity of phytoplankton not only influenced its own temporal stability, but also affected the stability of zooplankton through trophic interactions.

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Section: Discussionmentioning

confidence: 73%

Plankton Community Stability and Its Relationship with Phytoplankton Species Richness in Lake Nansihu, China

Zhang

Zhao

et al. 2016

Water

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“…Grazing affects both mortality and population structure (8), as has recently been observed in the rapid decline of biomass of Microcystis in a natural pond and in the restructuring of the bloom with a shift from a susceptible Microcystis species to a resistant one upon amoebal grazing (9). Whereas it is known that amoebae graze on cyanobacteria (10)(11)(12), these predators have not received much attention.…”

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confidence: 99%

“…Whereas it is known that amoebae graze on cyanobacteria (10)(11)(12), these predators have not received much attention. Van Wichelen et al (2010) attribute this omission to the fact that population densities of amoebae peak for short periods of time and, hence, may be overlooked during monthly or even biweekly samplings of freshwater environments (9).…”

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confidence: 99%

Impairment of O-antigen production confers resistance to grazing in a model amoeba–cyanobacterium predator–prey system

Simkovsky

Daniels

Tang³

et al. 2012

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

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The grazing activity of predators on photosynthetic organisms is a major mechanism of mortality and population restructuring in natural environments. Grazing is also one of the primary difficulties in growing cyanobacteria and other microalgae in large, open ponds for the production of biofuels, as contaminants destroy valuable biomass and prevent stable, continuous production of biofuel crops. To address this problem, we have isolated a heterolobosean amoeba, HGG1, that grazes upon unicellular and filamentous freshwater cyanobacterial species. We have established a model predator–prey system using this amoeba and Synechococcus elongatus PCC 7942. Application of amoebae to a library of mutants of S. elongatus led to the identification of a grazer-resistant knockout mutant of the wzm ABC O-antigen transporter gene, SynPCC7942_1126. Mutations in three other genes involved in O-antigen synthesis and transport also prevented the expression of O-antigen and conferred resistance to HGG1. Complementation of these rough mutants returned O-antigen expression and susceptibility to amoebae. Rough mutants are easily identifiable by appearance, are capable of autoflocculation, and do not display growth defects under standard laboratory growth conditions, all of which are desired traits for a biofuel production strain. Thus, preventing the production of O-antigen is a pathway for producing resistance to grazing by certain amoebae.

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“…As such, grazing on cyanobacteria is a major process at the base of food webs in these environments, and amoebae are among the natural grazers of cyanobacteria (22)(23)(24). As part of our efforts to understand the grazing process, we recently isolated a diverse set of amoebae that can be propagated using cyanobacterial species as prey (25).…”

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confidence: 99%

An Amoebal Grazer of Cyanobacteria Requires Cobalamin Produced by Heterotrophic Bacteria

Beld

Brahamsha

2017

Appl Environ Microbiol

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Amoebae are unicellular eukaryotes that consume microbial prey through phagocytosis, playing a role in shaping microbial food webs. Many amoebal species can be cultivated axenically in rich media or monoxenically with a single bacterial prey species. Here, we characterize heterolobosean amoeba LPG3, a recent natural isolate, which is unable to grow on unicellular cyanobacteria, its primary food source, in the absence of a heterotrophic bacterium, a Pseudomonas species coisolate. To investigate the molecular basis of this requirement for heterotrophic bacteria, we performed a screen using the defined nonredundant transposon library of Vibrio cholerae, which implicated genes in corrinoid uptake and biosynthesis. Furthermore, cobalamin synthase deletion mutations in V. cholerae and the Pseudomonas species coisolate do not support the growth of amoeba LPG3 on cyanobacteria. While cyanobacteria are robust producers of a corrinoid variant called pseudocobalamin, this variant does not support the growth of amoeba LPG3. Instead, we show that it requires cobalamin that is produced by the Pseudomonas species coisolate. The diversity of eukaryotes utilizing corrinoids is poorly understood, and this amoebal corrinoid auxotroph serves as a model for examining predator-prey interactions and micronutrient transfer in bacterivores underpinning microbial food webs.IMPORTANCE Cyanobacteria are important primary producers in aquatic environments, where they are grazed upon by a variety of phagotrophic protists and, hence, have an impact on nutrient flux at the base of microbial food webs. Here, we characterize amoebal isolate LPG3, which consumes cyanobacteria as its primary food source but also requires heterotrophic bacteria as a source of corrinoid vitamins. Amoeba LPG3 specifically requires the corrinoid variant produced by heterotrophic bacteria and cannot grow on cyanobacteria alone, as they produce a different corrinoid variant. This same corrinoid specificity is also exhibited by other eukaryotes, including humans and algae. This amoebal model system allows us to dissect predator-prey interactions to uncover factors that may shape microbial food webs while also providing insight into corrinoid specificity in eukaryotes.KEYWORDS amoeba, corrinoids, microbial interactions, vitamin B 12 U nicellular organisms dominate the eukaryotic phylogenetic tree of life. Although protists make up a significant part of natural microbial communities, they have been largely overlooked and are understudied as simple model eukaryotes (1, 2). While culture-independent metagenomic studies provide insight into the abundance and natural diversity of protists in environmental settings (3), in-depth characterization requires the isolation and cultivation of individual species. A large range of eukaryotic microalgal species have been cultivated and studied, particularly as a source of renewable biofuel compounds in recent years (4, 5); however, besides microalgae, there are only a few protist microbes developed as model systems. Amoebae are...

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Strong effects of amoebae grazing on the biomass and genetic structure of a Microcystis bloom (Cyanobacteria)

Cited by 55 publications

References 91 publications

Plankton Community Stability and Its Relationship with Phytoplankton Species Richness in Lake Nansihu, China

Plankton Community Stability and Its Relationship with Phytoplankton Species Richness in Lake Nansihu, China

Impairment of O-antigen production confers resistance to grazing in a model amoeba–cyanobacterium predator–prey system

An Amoebal Grazer of Cyanobacteria Requires Cobalamin Produced by Heterotrophic Bacteria

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