Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids.

Lai, Chi-Yung; Baumann, Linda C.; Baumann, Paul

doi:10.1073/pnas.91.9.3819

Cited by 140 publications

(177 citation statements)

References 39 publications

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“…Similarly, selection generally favors Buchnera mutations that increase host fecundity, because Buchnera relies on host reproduction for its own persistence. Such selection for mutualistic traits appears to underlie many observed features of the Buchnera genome, including retention of amino acid biosynthetic pathways (24), and amplification of some amino acid biosynthetic genes on plasmids (31). Aphids also exhibit symbiotic adaptations including bacteriocyte-specific expression of genes involved in amino acid metabolism and altered function of specific amino acid transporters within bacteriocytes (21,25,32).…”

Section: Discussionmentioning

confidence: 99%

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Chong

Moran

2016

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

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Symbiotic relationships promote biological diversification by unlocking new ecological niches. Over evolutionary time, hosts and symbionts often enter intimate and permanent relationships, which must be maintained and regulated for both lineages to persist. Many insect species harbor obligate, heritable symbiotic bacteria that provision essential nutrients and enable hosts to exploit niches that would otherwise be unavailable. Hosts must regulate symbiont population sizes, but optimal regulation may be affected by the need to respond to the ongoing evolution of symbionts, which experience high levels of genetic drift and potential selection for selfish traits. We address the extent of intraspecific variation in the regulation of a mutually obligate symbiosis, between the pea aphid (Acyrthosiphon pisum) and its maternally transmitted symbiont, Buchnera aphidicola. Using experimental crosses to identify effects of host genotypes, we measured symbiont titer, as the ratio of genomic copy numbers of symbiont and host, as well as developmental time and fecundity of hosts. We find a large (>10-fold) range in symbiont titer among genetically distinct aphid lines harboring the same Buchnera haplotype. Aphid clones also vary in fitness, measured as developmental time and fecundity, and genetically based variation in titer is correlated with host fitness, with higher titers corresponding to lower reproductive rates of hosts. Our work shows that obligate symbiosis is not static but instead is subject to short-term evolutionary dynamics, potentially reflecting coevolutionary interactions between host and symbiont.

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Section: Discussionmentioning

confidence: 99%

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Chong

Moran

2016

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

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“…Insects cannot synthesize aromatic amino acids and acquisition from diet and/or provisioning by endosymbionts is a common phenomenon. For example, B. aphidicola has evolved overproduction of phenylalanine and tryptophan (Lai et al, 1994;Jiménez et al, 2000). Similarly, B. floridanus can synthesize tyrosine, and increased tyrosine biosynthesis during the host's pupal stage (Zientz et al, 2006) coincides with elevated Blochmannia titers (Stoll et al, 2010;Ratzka et al, 2013).…”

Section: Westeberhardia As a Possible Source Of A Hgt Eventmentioning

confidence: 99%

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

et al. 2015

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The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant Cardiocondyla obscurior, 'Candidatus Westeberhardia cardiocondylae'. Upon metamorphosis, Westeberhardia is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain Westeberhardia in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of Westeberhardia (533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of Westeberhardia during pupal stage, this suggests a contribution of Westeberhardia to cuticle formation. Despite a widespread occurrence of Westeberhardia across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of C. obscurior.

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“…During this coevolutionary process, Buchnera suffered considerable genomic changes (i.e., a great reduction in genome size, an increased AϩT bias, great accumulation of deleterious mutations, and the amplification of genes involved in amino acid biosynthesis) (16)(17)(18). Because pathogenic intracellular bacteria with small genomes display a wide variation in chromosome length, it would also be expected that Buchnera of different aphid lineages differ in genome size and gene content.…”

mentioning

confidence: 99%

Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life

Gil

Sabater-Muñoz

Latorre

et al. 2002

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

206

142

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Buchnera is a mutualistic intracellular symbiont of aphids. Their association began about 200 million years ago, with host and symbiont lineages evolving in parallel since that time. During this coevolutionary process, Buchnera has experienced a dramatic decrease of genome size, retaining only essential genes for its specialized lifestyle. Previous studies reported that genome size in Buchnera spp. is very uniform, suggesting that genome shrinkage occurred early in evolution, and that modern lineages retain the genome size of a common ancestor. Our physical mapping of Buchnera genomes obtained from five aphid lineages shows that the genome size is not conserved among them, but has been reduced down to 450 kb in some species. Here we show evidence of six species with a genome size smaller than Mycoplasma genitalium, the smallest bacterial genome reported thus far (580 kb). Our findings strongly suggest that the Buchnera genome is still experiencing a reductive process toward a minimum set of genes necessary for its symbiotic lifestyle.

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Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids.

Abstract: Survival of aphids is dependent on an association with a prokaryotic endosymbiont (Buchnera aphidicola)

Cited by 140 publications

References 39 publications

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life

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