AUTHOR=Ravenscraft Alison , Thairu Margaret W. , Hansen Allison K. , Hunter Martha S. 

TITLE=Continent-Scale Sampling Reveals Fine-Scale Turnover in a Beneficial Bug Symbiont

JOURNAL=Frontiers in Microbiology

VOLUME=11

YEAR=2020

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2020.01276

DOI=10.3389/fmicb.2020.01276

ISSN=1664-302X

ABSTRACT=<p>Many members of animal-associated microbial communities, including the gut flora, are acquired from their host’s environment. While many of these communities are species rich, some true bugs (Hemiptera) in the superfamilies Lygaeoidea and Coreidae allow only ingested <italic>Burkholderia</italic> to colonize and reproduce in a large portion of the midgut. We studied the spatial structuring of <italic>Burkholderia</italic> associated with a widespread omnivorous bug genus, <italic>Jalysus</italic> (Berytidae). We sampled Wickham’s stilt bug, <italic>Jalysus wickhami</italic>, across the United States and performed limited sampling of its sister species, the spined stilt bug <italic>Jalysus spinosus</italic>. We asked: (1) What <italic>Burkholderia</italic> strains are hosted by <italic>Jalysus</italic> at different locations? (2) Does host insect species, host plant species, or location influence the strain these insects acquire? (3) How does <italic>Burkholderia</italic> affect the development and reproductive fitness of <italic>J. wickhami</italic>? We found: (1) Sixty-one <italic>Burkholderia</italic> strains were present across a sample of 352 individuals, but one strain dominated, accounting for almost half of all symbiont reads. Most strains were closely related to other hemipteran <italic>Burkholderia</italic> symbionts. (2) Many individuals hosted more than one strain of <italic>Burkholderia</italic>. (3) <italic>J. wickhami</italic> and <italic>J. spinosus</italic> did not differ in the strains they hosted. (4) Insects that fed on different plant species tended to host different <italic>Burkholderia</italic>, but this accounted for only 4% of the variation in strains hosted. In contrast, the location at which an insect was collected explained 27% of the variation in symbiont strains. (5) <italic>Burkholderia</italic> confers important fitness benefits to <italic>J. wickhami.</italic> In laboratory experiments, aposymbiotic (<italic>Burkholderia</italic>-free) insects developed more slowly and laid fewer eggs than symbiotic (<italic>Burkholderia-</italic>colonized) insects. (6) In the lab, nymphs sometimes acquired <italic>Burkholderia</italic> via indirect exposure to adults, indicating that horizontal symbiont transmission can occur via adult insect-mediated enrichment of <italic>Burkholderia</italic> in the local environment – a phenomenon not previously reported in bug-<italic>Burkholderia</italic> relationships. Taken together, the results suggest that for these bugs, critical nutritional requirements are outsourced to a highly diverse and spatially structured collection of <italic>Burkholderia</italic> strains acquired from the environment and, occasionally, from conspecific adults.</p>