Diversity of Bacterial Endosymbionts of Environmental
            <i>Acanthamoeba</i>
            Isolates

Schmitz‐Esser, Stephan; Toenshoff, Elena R.; Haider, Susanne; Heinz, Eva; Hoenninger, Verena M.; Wagner, Michael; Horn, Matthias

doi:10.1128/aem.01093-08

Cited by 93 publications

(114 citation statements)

References 53 publications

(62 reference statements)

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“…The amoeba containing "Ca. Amoebophilus asiaticus" 5a2 (ATCC number PRA-228) was isolated from lake sediment in Austria (107) (107). Cultures were incubated at 30°C; fresh medium was applied every 5 to 10 days.…”

Section: Methodsmentioning

confidence: 99%

“…These obligate amoeba symbionts show a worldwide distribution, since phylogenetically highly similar strains were found in amoeba isolates from geographically distant sources (51,107). The phylogenetic diversity and the different lifestyles of these obligate intracellular bacteriasome are located directly in the host cell cytoplasm (11,34,(48)(49)(50)52), while others are enclosed in host-derived vacuoles (4,35,44)-suggest fundamentally different mechanisms of host cell interaction.…”

mentioning

confidence: 99%

“…"Ca. Amoebophilus asiaticus" is a Gram-negative, obligate intracellular amoeba symbiont belonging to the Bacteroidetes which has been discovered within an amoeba isolated from lake sediment (107). "Ca.…”

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confidence: 99%

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The Genome of the Amoeba Symbiont “CandidatusAmoebophilus asiaticus” Reveals Common Mechanisms for Host Cell Interaction among Amoeba-Associated Bacteria

et al. 2010

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Protozoa play host for many intracellular bacteria and are important for the adaptation of pathogenic bacteria to eukaryotic cells. We analyzed the genome sequence of "Candidatus Amoebophilus asiaticus," an obligate intracellular amoeba symbiont belonging to the Bacteroidetes. The genome has a size of 1.89 Mbp, encodes 1,557 proteins, and shows massive proliferation of IS elements (24% of all genes), although the genome seems to be evolutionarily relatively stable. The genome does not encode pathways for de novo biosynthesis of cofactors, nucleotides, and almost all amino acids. "Ca. Amoebophilus asiaticus" encodes a variety of proteins with predicted importance for host cell interaction; in particular, an arsenal of proteins with eukaryotic domains, including ankyrin-, TPR/SEL1-, and leucine-rich repeats, which is hitherto unmatched among prokaryotes, is remarkable. Unexpectedly, 26 proteins that can interfere with the host ubiquitin system were identified in the genome. These proteins include F-and U-box domain proteins and two ubiquitin-specific proteases of the CA clan C19 family, representing the first prokaryotic members of this protein family. Consequently, interference with the host ubiquitin system is an important host cell interaction mechanism of "Ca. Amoebophilus asiaticus". More generally, we show that the eukaryotic domains identified in "Ca. Amoebophilus asiaticus" are also significantly enriched in the genomes of other amoeba-associated bacteria (including chlamydiae, Legionella pneumophila, Rickettsia bellii, Francisella tularensis, and Mycobacterium avium). This indicates that phylogenetically and ecologically diverse bacteria which thrive inside amoebae exploit common mechanisms for interaction with their hosts, and it provides further evidence for the role of amoebae as training grounds for bacterial pathogens of humans.Free-living amoebae, such as Acanthamoeba spp., are ubiquitous protozoa which can be found in such diverse habitats as soil, marine water, and freshwater and in many engineered environments (62, 100). They are important predators of prokaryotic and eukaryotic microorganisms, thereby having great influence on microbial community composition, soil mineralization, plant growth, and nutrient cycles (14, 100). Interestingly, many well-known pathogens of humans are able to infect, survive, and multiply within amoebae (39, 51). These protozoa can thus serve as reservoirs and vectors for the transmission of pathogenic bacteria to humans, as demonstrated for L. pneumophila and Mycobacterium avium (2, 115). It is also increasingly being recognized that protozoa are important for the adaptation of (pathogenic) bacteria to higher eukaryotic cells as a niche for growth (2,24,42,78,89).In addition to the many recognized transient associations between amoeba and pathogens, stable and obligate relationships between bacteria and amoebae also were described for members of the Alphaproteobacteria (11, 34, 48), the Betaproteobacteria (49), the Bacteroidetes (50), and the Chlamydiae (4, 12, 35, 52...

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Section: Methodsmentioning

confidence: 99%

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confidence: 99%

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The Genome of the Amoeba Symbiont “CandidatusAmoebophilus asiaticus” Reveals Common Mechanisms for Host Cell Interaction among Amoeba-Associated Bacteria

et al. 2010

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“…Odyssella" and "Ca. Paracaedibacter" (37)(38)(39), it seems likely that the electron-dense outer layer surrounding "Ca. Finniella" does not represent a host-derived membrane.…”

Section: Phylogenetic Identity and Taxonomy Of "Candidatus Finniella"mentioning

confidence: 99%

“Candidatus Finniella” (Rickettsiales, Alphaproteobacteria), Novel Endosymbionts of Viridiraptorid Amoeboflagellates (Cercozoa, Rhizaria)

Hess

Suthaus

Melkonian

2016

Appl Environ Microbiol

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The Rickettsiales (Alphaproteobacteria) are obligate intracellular bacteria that colonize a wide range of eukaryotic hosts, including diverse metazoa and protists. Here, we characterize rickettsial endosymbionts discovered in the cytoplasm of the algivorous amoeboflagellates Viridiraptor invadens and Orciraptor agilis (Viridiraptoridae, Cercozoa, Rhizaria), supplying evidence of free-living, phagotrophic members of the Cercozoa serving as hosts for Rickettsiales. According to 16S rRNA gene phylogenies, the bacteria represent two closely related but distinct genotypes within a deep-branching rickettsial clade, which contains the genera "Candidatus Odyssella," "Candidatus Paracaedibacter," and "Candidatus Captivus." Using the full-cycle rRNA approach, we detected the novel bacteria in four of nine viridiraptorid strains tested. Furthermore, two specific oligonucleotide probes with a single-nucleotide-difference discriminated both bacterial genotypes by fluorescence in situ hybridization (FISH). We establish the candidate species "Candidatus Finniella inopinata" (found in Viridiraptor invadens) and "Candidatus Finniella lucida" (found in Orciraptor agilis) for the novel bacteria and propose a new, provisional family of Rickettsiales, "Candidatus Paracaedibacteraceae." T he family Viridiraptoridae (Cercozoa, Rhizaria) comprises amoeboflagellates that perforate the cell walls of freshwater green algae (Viridiplantae) and feed on the algal cell contents by phagocytosis (1). During the ultrastructural investigation of Viridiraptor invadens, we observed intracellular bacteria that were scattered throughout the cytoplasm and not enclosed in a vacuolar membrane (2). Besides these ultrastructural features, the strictly algivorous diet of Viridiraptor and the axenic culture conditions excluded the possibility of engulfed food bacteria and instead suggested that Viridiraptor was colonized by endosymbionts. Singlecelled eukaryotes (protists) of diverse phylogenetic affiliations are known to harbor bacterial endosymbionts and therefore represent an almost ubiquitous, natural reservoir for facultative and obligate intracellular bacteria (3-5). The bacteria colonizing eukaryotic cells are equally diverse, and a broad spectrum of interaction exists, ranging from mutualism and balanced parasitism to pathogenic situations that involve host cell lysis (5). Protists have even been suggested to serve as vectors and training grounds for pathogenic bacteria (6). They are frequently colonized by representatives of the eubacterial orders Chlamydiales (Chlamydiae), Legionellales (Gammaproteobacteria), and Rickettsiales (Alphaproteobacteria), whose members are linked to severe diseases in mammals, including humans (7-9).Compared to other protist groups, such as ciliates (Alveolata) and bacterivorous amoebae (Amoebozoa), Rhizaria are poorly studied in terms of endosymbiotic relationships with heterotrophic bacteria. Therefore, our finding triggered the following questions. What is the phylogenetic affiliation of the bacteria residing in Viri...

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“…The strains were classified to genotype according to the 95% sequence similarity threshold for 18S rRNA genes (27) using standard methods (11,13). All strains were members of sequence type T4 (24), with the exception of Acanthamoeba sp. strain F2B (type T13) and Acanthamoeba hatchetii (type 11) (GenBank accession no.…”

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Mycobacterium avium Infections of Acanthamoeba Strains: Host Strain Variability, Grazing-Acquired Infections, and Altered Dynamics of Inactivation with Monochloramine

Berry

Horn

et al. 2010

Appl Environ Microbiol

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Stable Mycobacterium avium infections of several Acanthamoeba strains were characterized by increased infection resistance of recent environmental isolates and reduced infectivity in the presence of other bacteria. Exposure of M. avium in coculture with Acanthamoeba castellanii to monochloramine yielded inactivation kinetics markedly similar to those observed for A. castellanii alone.Acanthamoebae are widely distributed in the environment (20) and generally function ecologically as predators of bacteria (23), although numerous types of bacteria resist predation (22). Acanthamoebae are very resistant to a range of disinfectants (5,6,8,28), and bacteria within acanthamoebae are generally afforded extra protection (16). A notable example is the opportunistic pathogen Mycobacterium avium (10), which can survive within Acanthamoeba species trophozoites and cysts (4, 26), resulting in increased resistance to several antimicrobials (22). It has been demonstrated that many Mycobacterium spp. are able to infect the laboratory strain Acanthamoeba polyphaga (1). Acanthamoeba cultures undergo many physiological changes after several passages in the laboratory (15,17,21), although it is not known if prolonged cultivation of Acanthamoeba alters their capacity to be infected by M. avium. This knowledge is important for assessing the environmental relevance of associations between Acanthamoeba and M. avium. Therefore, we studied the infectivity and infection stability of M. avium with several laboratory and environmental Acanthamoeba strains for 28 days under high-nutrient (peptone-yeast extract-glucose [PYG] medium) and low-nutrient (Page's amoeba saline [PAS]) conditions. M. avium infections in different Acanthamoeba strains. Eight Acanthamoeba strains were studied, four of which were recently isolated from the environment (biofilm from a drinking water distribution system, forest soil, and two from marsh sediment) and four "laboratory strains" which had been passaged many times on nutrient-rich medium (see Table S1 in the supplemental material). Fresh isolates (Ͻ2 months) were passaged no more than three times and were determined to be free of endosymbionts and acid-fast stained structures, by the use of methods described previously (13). The strains were classified to genotype according to the 95% sequence similarity threshold for 18S rRNA genes (27) using standard methods (11, 13). All strains were members of sequence type T4 (24), with the exception of Acanthamoeba sp. strain F2B (type T13) and Acanthamoeba hatchetii (type 11) (GenBank accession no. FJ807647 to FJ807651) (see Fig. S1 in the supplemental material). Mycobacterium avium subsp. hominissuis 104 (2) was cultured on Middlebrook 7H9/OADC (oleic acid-albumin-dextrose-catalase) broth (Sigma-Aldrich). M. avium was added to Acanthamoeba monolayers at a multiplicity of infection of 10:1 and treated with amikacin as described previously (4). Cocultures were incubated at 20°C in the dark and were washed and treated weekly with amikacin to minimize the potential for extr...

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Diversity of Bacterial Endosymbionts of Environmental Acanthamoeba Isolates

Cited by 93 publications

References 53 publications

The Genome of the Amoeba Symbiont “CandidatusAmoebophilus asiaticus” Reveals Common Mechanisms for Host Cell Interaction among Amoeba-Associated Bacteria

The Genome of the Amoeba Symbiont “CandidatusAmoebophilus asiaticus” Reveals Common Mechanisms for Host Cell Interaction among Amoeba-Associated Bacteria

“Candidatus Finniella” (Rickettsiales, Alphaproteobacteria), Novel Endosymbionts of Viridiraptorid Amoeboflagellates (Cercozoa, Rhizaria)

Mycobacterium avium Infections of Acanthamoeba Strains: Host Strain Variability, Grazing-Acquired Infections, and Altered Dynamics of Inactivation with Monochloramine

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