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The earthworm-Verminephrobacter symbiosis: an emerging experimental system to study extracellular symbiosis.

Lund MB, Kjeldsen KU, Schramm A - Front Microbiol (2014)

Bottom Line: Lumbricidae) harbor extracellular species-specific bacterial symbionts of the genus Verminephrobacter (Betaproteobacteria) in their nephridia.The symbionts have a beneficial effect on host reproduction and likely live on their host's waste products.We propose that the opportunity for genetic mixing during part of the host-symbiont life cycle is the key to evade drift-induced genome erosion.

View Article: PubMed Central - PubMed

Affiliation: Aarhus Institute of Advanced Studies, Aarhus University Aarhus, Denmark.

ABSTRACT

Almost all lumbricid earthworms (oligochaeta: Lumbricidae) harbor extracellular species-specific bacterial symbionts of the genus Verminephrobacter (Betaproteobacteria) in their nephridia. The symbionts have a beneficial effect on host reproduction and likely live on their host's waste products. They are vertically transmitted and presumably associated with earthworms already at the origin of Lumbricidae 62-136 million years ago. The Verminephrobacter genomes carry signs of bottleneck-induced genetic drift, such as accelerated evolutionary rates, low codon usage bias, and extensive genome shuffling, which are characteristic of vertically transmitted intracellular symbionts. However, the Verminephrobacter genomes lack AT bias, size reduction, and pseudogenization, which are also common genomic hallmarks of vertically transmitted, intracellular symbionts. We propose that the opportunity for genetic mixing during part of the host-symbiont life cycle is the key to evade drift-induced genome erosion. Furthermore, we suggest the earthworm-Verminephrobacter association as a new experimental system for investigating host-microbe interactions, and especially for understanding genome evolution of vertically transmitted symbionts in the presence of genetic mixing.

No MeSH data available.


Related in: MedlinePlus

Genome evolution of vertically transmitted symbionts after host restriction. The scope for genetic mixing has large implications for symbiont genome evolution. (A) Genome evolution of vertically transmitted symbionts experiencing environmental fluctuations during the host—symbiont life cycle and with the opportunity for genetic mixing. (B) Genome evolution of vertically transmitted symbionts living in genetic isolation (Panel (B) redrawn from McCutcheon and Moran, 2012).
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Figure 2: Genome evolution of vertically transmitted symbionts after host restriction. The scope for genetic mixing has large implications for symbiont genome evolution. (A) Genome evolution of vertically transmitted symbionts experiencing environmental fluctuations during the host—symbiont life cycle and with the opportunity for genetic mixing. (B) Genome evolution of vertically transmitted symbionts living in genetic isolation (Panel (B) redrawn from McCutcheon and Moran, 2012).

Mentions: Interestingly, the genome of V. eiseniae has no synteny to the genomes of two closely related Acidovorax species (Pinel, 2009), or the large contigs of the partially sequenced symbiont of the earthworm A. tuberculata (Figure S1), which indicates that the Verminephrobacter genomes are actively rearranging. This is supported by the very low DNA–DNA hybridization values found between three strains of Verminephrobacter symbionts from different earthworm hosts (28.3–58.8%) (Lund et al., 2011). V. eiseniae also contains a high number of palindromic repeats and insertion sequence elements; about 2.3% of its genome is comprised of one type of palindromic repeat, VeiPR1, unique to V. eiseniae (Pinel, 2009). A high load of mobile DNA is expected in organisms that have recently transitioned to an obligate intracellular lifestyle (Moran and Plague, 2004), as bottleneck-induced genetic drift will allow mobile genetic elements to proliferate in the genome. However, with time, mobile DNA elements will be inactivated and lost, and new mobile elements can only be acquired through recombination with other organisms (Figure 2B). This explains the almost total absence of mobile DNA in old obligate insect endosymbionts and the high number of mobile elements in more recent obligate host associates (Moran and Plague, 2004; Bordenstein and Reznikoff, 2005; Moran et al., 2009). According to this theory the earthworm—Verminephrobacter symbiosis resembles a young symbiosis in transition toward genome reduction; however, low pseudogenization (Pinel, 2009), overall strong purifying selection (Kjeldsen et al., 2012), and a high age of the symbiosis (62–136 MY, Bouché, 1983; Lund et al., 2010a) do not support this theory.


The earthworm-Verminephrobacter symbiosis: an emerging experimental system to study extracellular symbiosis.

Lund MB, Kjeldsen KU, Schramm A - Front Microbiol (2014)

Genome evolution of vertically transmitted symbionts after host restriction. The scope for genetic mixing has large implications for symbiont genome evolution. (A) Genome evolution of vertically transmitted symbionts experiencing environmental fluctuations during the host—symbiont life cycle and with the opportunity for genetic mixing. (B) Genome evolution of vertically transmitted symbionts living in genetic isolation (Panel (B) redrawn from McCutcheon and Moran, 2012).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3975124&req=5

Figure 2: Genome evolution of vertically transmitted symbionts after host restriction. The scope for genetic mixing has large implications for symbiont genome evolution. (A) Genome evolution of vertically transmitted symbionts experiencing environmental fluctuations during the host—symbiont life cycle and with the opportunity for genetic mixing. (B) Genome evolution of vertically transmitted symbionts living in genetic isolation (Panel (B) redrawn from McCutcheon and Moran, 2012).
Mentions: Interestingly, the genome of V. eiseniae has no synteny to the genomes of two closely related Acidovorax species (Pinel, 2009), or the large contigs of the partially sequenced symbiont of the earthworm A. tuberculata (Figure S1), which indicates that the Verminephrobacter genomes are actively rearranging. This is supported by the very low DNA–DNA hybridization values found between three strains of Verminephrobacter symbionts from different earthworm hosts (28.3–58.8%) (Lund et al., 2011). V. eiseniae also contains a high number of palindromic repeats and insertion sequence elements; about 2.3% of its genome is comprised of one type of palindromic repeat, VeiPR1, unique to V. eiseniae (Pinel, 2009). A high load of mobile DNA is expected in organisms that have recently transitioned to an obligate intracellular lifestyle (Moran and Plague, 2004), as bottleneck-induced genetic drift will allow mobile genetic elements to proliferate in the genome. However, with time, mobile DNA elements will be inactivated and lost, and new mobile elements can only be acquired through recombination with other organisms (Figure 2B). This explains the almost total absence of mobile DNA in old obligate insect endosymbionts and the high number of mobile elements in more recent obligate host associates (Moran and Plague, 2004; Bordenstein and Reznikoff, 2005; Moran et al., 2009). According to this theory the earthworm—Verminephrobacter symbiosis resembles a young symbiosis in transition toward genome reduction; however, low pseudogenization (Pinel, 2009), overall strong purifying selection (Kjeldsen et al., 2012), and a high age of the symbiosis (62–136 MY, Bouché, 1983; Lund et al., 2010a) do not support this theory.

Bottom Line: Lumbricidae) harbor extracellular species-specific bacterial symbionts of the genus Verminephrobacter (Betaproteobacteria) in their nephridia.The symbionts have a beneficial effect on host reproduction and likely live on their host's waste products.We propose that the opportunity for genetic mixing during part of the host-symbiont life cycle is the key to evade drift-induced genome erosion.

View Article: PubMed Central - PubMed

Affiliation: Aarhus Institute of Advanced Studies, Aarhus University Aarhus, Denmark.

ABSTRACT

Almost all lumbricid earthworms (oligochaeta: Lumbricidae) harbor extracellular species-specific bacterial symbionts of the genus Verminephrobacter (Betaproteobacteria) in their nephridia. The symbionts have a beneficial effect on host reproduction and likely live on their host's waste products. They are vertically transmitted and presumably associated with earthworms already at the origin of Lumbricidae 62-136 million years ago. The Verminephrobacter genomes carry signs of bottleneck-induced genetic drift, such as accelerated evolutionary rates, low codon usage bias, and extensive genome shuffling, which are characteristic of vertically transmitted intracellular symbionts. However, the Verminephrobacter genomes lack AT bias, size reduction, and pseudogenization, which are also common genomic hallmarks of vertically transmitted, intracellular symbionts. We propose that the opportunity for genetic mixing during part of the host-symbiont life cycle is the key to evade drift-induced genome erosion. Furthermore, we suggest the earthworm-Verminephrobacter association as a new experimental system for investigating host-microbe interactions, and especially for understanding genome evolution of vertically transmitted symbionts in the presence of genetic mixing.

No MeSH data available.


Related in: MedlinePlus