Affiliation:
1. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan
2. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan
3. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
Abstract
ABSTRACT
Diverse insects are intimately associated with specific symbiotic bacteria, where host and symbiont are integrated into an almost inseparable biological entity. These symbiotic bacteria usually exhibit host specificity, uncultivability, reduced genome size, and other peculiar traits relevant to their symbiotic lifestyle. How host-symbiont specificity is established at the very beginning of symbiosis is of interest but poorly understood. To gain insight into the evolutionary issue, we adopted an experimental approach using the recently developed evolutionary model of symbiosis between the stinkbug
Plautia stali
and
Escherichia coli
. Based on the laboratory evolution of
P. stali-E. coli
mutualism, we selected Δ
cyaA
mutant of
E. coli
as an artificial symbiont of
P. stali
that has established mutualism by a single mutation. In addition, we selected a natural cultivable symbiont of
P. stali
of relatively recent evolutionary origin. These artificial and natural symbiotic bacteria of
P. stali
were experimentally inoculated to symbiont-deprived newborn nymphs of diverse stinkbug species. Strikingly, the mutualistic
E. coli
was unable to establish infection and support growth and survival of all the stinkbug species except for
P. stali
, uncovering that host specificity can be established at a very early stage of symbiotic evolution. Meanwhile, the natural symbiont was able to establish infection and support growth and survival of several stinkbug species in addition to
P. stali
, unveiling that a broader host range of the symbiont has evolved in nature. Based on these findings, we discuss what factors are relevant to the establishment of host specificity in the evolution of symbiosis.
IMPORTANCE
How does host-symbiont specificity emerge at the very beginning of symbiosis? This question is difficult to address because it is generally difficult to directly observe the onset of symbiosis. However, recent development of experimental evolutionary approaches to symbiosis has brought about a breakthrough. Here we tackled this evolutionary issue using a symbiotic
Escherichia coli
created in laboratory and a natural
Pantoea
symbiont, which are both mutualistic to the stinkbug
Plautia stali
. We experimentally replaced essential symbiotic bacteria of diverse stinkbugs with the artificial and natural symbionts of
P. stali
and evaluated whether the symbiotic bacteria, which evolved for a specific host, can establish infection and support the growth and survival of heterospecific hosts. Strikingly, the artificial symbiont showed strict host specificity to
P. stali
, whereas the natural symbiont was capable of symbiosis with diverse stinkbugs, which provide insight into how host-symbiont specificity can be established at early evolutionary stages of symbiosis.
Funder
MEXT | Japan Science and Technology Agency
Publisher
American Society for Microbiology
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