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Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution.

Nováková E, Hypsa V, Moran NA - BMC Microbiol. (2009)

Bottom Line: A further conspicuous feature of the topology is the occurrence of monophyletic symbiont lineages associated with monophyletic groups of hosts without a co-speciation pattern.However, under the current practice, relying exclusively on 16S rRNA sequences, the phylogenetic analyses are sensitive to various methodological artifacts that may even lead to description of new Arsenophonus lineages as independent genera (e.g. Riesia and Phlomobacter).The resolution of the evolutionary questions encountered within the Arsenophonus clade will thus require identification of new molecular markers suitable for the low-level phylogenetics.

View Article: PubMed Central - HTML - PubMed

Affiliation: Faculty of Science, University of South Bohemia, Branisovská 31, Ceské Budejovice 37005, Czech Republic. novaeva@paru.cas.cz

ABSTRACT

Background: The genus Arsenophonus is a group of symbiotic, mainly insect-associated bacteria with rapidly increasing number of records. It is known from a broad spectrum of hosts and symbiotic relationships varying from parasitic son-killers to coevolving mutualists.The present study extends the currently known diversity with 34 samples retrieved mainly from hippoboscid (Diptera: Hippoboscidae) and nycteribiid (Diptera: Nycteribiidae) hosts, and investigates phylogenetic relationships within the genus.

Results: The analysis of 110 Arsenophonus sequences (incl. Riesia and Phlomobacter), provides a robust monophyletic clade, characterized by unique molecular synapomorphies. On the other hand, unstable inner topology indicates that complete understanding of Arsenophonus evolution cannot be achieved with 16S rDNA. Moreover, taxonomically restricted Sampling matrices prove sensitivity of the phylogenetic signal to sampling; in some cases, Arsenophonus monophyly is disrupted by other symbiotic bacteria. Two contrasting coevolutionary patterns occur throughout the tree: parallel host-symbiont evolution and the haphazard association of the symbionts with distant hosts. A further conspicuous feature of the topology is the occurrence of monophyletic symbiont lineages associated with monophyletic groups of hosts without a co-speciation pattern. We suggest that part of this incongruence could be caused by methodological artifacts, such as intragenomic variability.

Conclusion: The sample of currently available molecular data presents the genus Arsenophonus as one of the richest and most widespread clusters of insect symbiotic bacteria. The analysis of its phylogenetic lineages indicates a complex evolution and apparent ecological versatility with switches between entirely different life styles. Due to these properties, the genus should play an important role in the studies of evolutionary trends in insect intracellular symbionts. However, under the current practice, relying exclusively on 16S rRNA sequences, the phylogenetic analyses are sensitive to various methodological artifacts that may even lead to description of new Arsenophonus lineages as independent genera (e.g. Riesia and Phlomobacter). The resolution of the evolutionary questions encountered within the Arsenophonus clade will thus require identification of new molecular markers suitable for the low-level phylogenetics.

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An increase of records on Arsenophonus bacteria from various insect groups. The bars show cumulative numbers of sequences deposited into GenBank; dark tops represent new records added in the given year. The sequences are identified with the following accession numbers: 1991 – M90801; 1997 – U91786; 2000 – AF263561, AF263562, AF286129, AB038366; 2001 – AF400474, AF400480, AF400481, AF400478, AY057392; 2002 – AY136168, AY136153, AY136142; 2003 – AY265341–AY265348, Y264663–AY264673, AY264677; 2004 – AY587141, AY587142, AY587140; 2005 – DQ068928, DQ314770–DQ314774, DQ314777, DQ314768, DQ115536; 2006 – DQ538372–DQ538379, DQ508171–DQ508186, DQ517447, DQ508193, DQ837612, DQ837613; 2007 – EU039464, EU043378, EF110573, EF110574, DQ076660, DQ076659, EF110572, EF647590, AB263104.
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Figure 1: An increase of records on Arsenophonus bacteria from various insect groups. The bars show cumulative numbers of sequences deposited into GenBank; dark tops represent new records added in the given year. The sequences are identified with the following accession numbers: 1991 – M90801; 1997 – U91786; 2000 – AF263561, AF263562, AF286129, AB038366; 2001 – AF400474, AF400480, AF400481, AF400478, AY057392; 2002 – AY136168, AY136153, AY136142; 2003 – AY265341–AY265348, Y264663–AY264673, AY264677; 2004 – AY587141, AY587142, AY587140; 2005 – DQ068928, DQ314770–DQ314774, DQ314777, DQ314768, DQ115536; 2006 – DQ538372–DQ538379, DQ508171–DQ508186, DQ517447, DQ508193, DQ837612, DQ837613; 2007 – EU039464, EU043378, EF110573, EF110574, DQ076660, DQ076659, EF110572, EF647590, AB263104.

Mentions: The bacterial genus Arsenophonus corresponds to a group of insect intracellular symbionts with a long history of investigation. Although many new Arsenophonus sequences have been published in the last several years, along with documentation of diverse evolutionary patterns in this group (Figure 1), the first records of these bacteria date to the pre-molecular era. Based on ultrastructural features, several authors described a transovarially transmitted infection associated with son-killing in the parasitoid wasp Nasonia vitripennis [1-3]. Later, they were formally assigned to a new genus within the family Enterobacteriaceae with a single species, Arsenophonus nasoniae [4]. The same authors proposed a close relationship of Arsenophonus to free-living bacteria of the genus Proteus. Independently, other microscopic studies revealed morphologically similar symbionts from various tissues of blood-sucking triatomine bugs [5,6]; a decade later these bacteria were determined on molecular grounds to belong to the same clade and were named Arsenophonus triatominarum [7]. Interestingly, the next record on symbiotic bacteria closely related to A. nasoniae was from a phytopathological study investigating marginal chlorosis of strawberry [8]. Since available sequence data were insufficient for reliable phylogenetic placement, the phloem-inhabiting pathogen was described as a new genus, Phlomobacter, with a single species P. fragariae [8].


Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution.

Nováková E, Hypsa V, Moran NA - BMC Microbiol. (2009)

An increase of records on Arsenophonus bacteria from various insect groups. The bars show cumulative numbers of sequences deposited into GenBank; dark tops represent new records added in the given year. The sequences are identified with the following accession numbers: 1991 – M90801; 1997 – U91786; 2000 – AF263561, AF263562, AF286129, AB038366; 2001 – AF400474, AF400480, AF400481, AF400478, AY057392; 2002 – AY136168, AY136153, AY136142; 2003 – AY265341–AY265348, Y264663–AY264673, AY264677; 2004 – AY587141, AY587142, AY587140; 2005 – DQ068928, DQ314770–DQ314774, DQ314777, DQ314768, DQ115536; 2006 – DQ538372–DQ538379, DQ508171–DQ508186, DQ517447, DQ508193, DQ837612, DQ837613; 2007 – EU039464, EU043378, EF110573, EF110574, DQ076660, DQ076659, EF110572, EF647590, AB263104.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2724383&req=5

Figure 1: An increase of records on Arsenophonus bacteria from various insect groups. The bars show cumulative numbers of sequences deposited into GenBank; dark tops represent new records added in the given year. The sequences are identified with the following accession numbers: 1991 – M90801; 1997 – U91786; 2000 – AF263561, AF263562, AF286129, AB038366; 2001 – AF400474, AF400480, AF400481, AF400478, AY057392; 2002 – AY136168, AY136153, AY136142; 2003 – AY265341–AY265348, Y264663–AY264673, AY264677; 2004 – AY587141, AY587142, AY587140; 2005 – DQ068928, DQ314770–DQ314774, DQ314777, DQ314768, DQ115536; 2006 – DQ538372–DQ538379, DQ508171–DQ508186, DQ517447, DQ508193, DQ837612, DQ837613; 2007 – EU039464, EU043378, EF110573, EF110574, DQ076660, DQ076659, EF110572, EF647590, AB263104.
Mentions: The bacterial genus Arsenophonus corresponds to a group of insect intracellular symbionts with a long history of investigation. Although many new Arsenophonus sequences have been published in the last several years, along with documentation of diverse evolutionary patterns in this group (Figure 1), the first records of these bacteria date to the pre-molecular era. Based on ultrastructural features, several authors described a transovarially transmitted infection associated with son-killing in the parasitoid wasp Nasonia vitripennis [1-3]. Later, they were formally assigned to a new genus within the family Enterobacteriaceae with a single species, Arsenophonus nasoniae [4]. The same authors proposed a close relationship of Arsenophonus to free-living bacteria of the genus Proteus. Independently, other microscopic studies revealed morphologically similar symbionts from various tissues of blood-sucking triatomine bugs [5,6]; a decade later these bacteria were determined on molecular grounds to belong to the same clade and were named Arsenophonus triatominarum [7]. Interestingly, the next record on symbiotic bacteria closely related to A. nasoniae was from a phytopathological study investigating marginal chlorosis of strawberry [8]. Since available sequence data were insufficient for reliable phylogenetic placement, the phloem-inhabiting pathogen was described as a new genus, Phlomobacter, with a single species P. fragariae [8].

Bottom Line: A further conspicuous feature of the topology is the occurrence of monophyletic symbiont lineages associated with monophyletic groups of hosts without a co-speciation pattern.However, under the current practice, relying exclusively on 16S rRNA sequences, the phylogenetic analyses are sensitive to various methodological artifacts that may even lead to description of new Arsenophonus lineages as independent genera (e.g. Riesia and Phlomobacter).The resolution of the evolutionary questions encountered within the Arsenophonus clade will thus require identification of new molecular markers suitable for the low-level phylogenetics.

View Article: PubMed Central - HTML - PubMed

Affiliation: Faculty of Science, University of South Bohemia, Branisovská 31, Ceské Budejovice 37005, Czech Republic. novaeva@paru.cas.cz

ABSTRACT

Background: The genus Arsenophonus is a group of symbiotic, mainly insect-associated bacteria with rapidly increasing number of records. It is known from a broad spectrum of hosts and symbiotic relationships varying from parasitic son-killers to coevolving mutualists.The present study extends the currently known diversity with 34 samples retrieved mainly from hippoboscid (Diptera: Hippoboscidae) and nycteribiid (Diptera: Nycteribiidae) hosts, and investigates phylogenetic relationships within the genus.

Results: The analysis of 110 Arsenophonus sequences (incl. Riesia and Phlomobacter), provides a robust monophyletic clade, characterized by unique molecular synapomorphies. On the other hand, unstable inner topology indicates that complete understanding of Arsenophonus evolution cannot be achieved with 16S rDNA. Moreover, taxonomically restricted Sampling matrices prove sensitivity of the phylogenetic signal to sampling; in some cases, Arsenophonus monophyly is disrupted by other symbiotic bacteria. Two contrasting coevolutionary patterns occur throughout the tree: parallel host-symbiont evolution and the haphazard association of the symbionts with distant hosts. A further conspicuous feature of the topology is the occurrence of monophyletic symbiont lineages associated with monophyletic groups of hosts without a co-speciation pattern. We suggest that part of this incongruence could be caused by methodological artifacts, such as intragenomic variability.

Conclusion: The sample of currently available molecular data presents the genus Arsenophonus as one of the richest and most widespread clusters of insect symbiotic bacteria. The analysis of its phylogenetic lineages indicates a complex evolution and apparent ecological versatility with switches between entirely different life styles. Due to these properties, the genus should play an important role in the studies of evolutionary trends in insect intracellular symbionts. However, under the current practice, relying exclusively on 16S rRNA sequences, the phylogenetic analyses are sensitive to various methodological artifacts that may even lead to description of new Arsenophonus lineages as independent genera (e.g. Riesia and Phlomobacter). The resolution of the evolutionary questions encountered within the Arsenophonus clade will thus require identification of new molecular markers suitable for the low-level phylogenetics.

Show MeSH
Related in: MedlinePlus