Thermal sensitivity of bacteriocytes constrains the persistence of intracellular bacteria in whitefly symbiosis under heat stress

Abstract

Temperature affects the persistence of diverse symbionts of insects. Our previous study indicates that the whitefly symbionts confined within bacteriocytes or scattered throughout the body cavity outside bacteriocytes may have differential thermal sensitivity. However, the underlying mechanisms remain largely unknown. Here, we report that following continuous heat stress, Portiera and Hamiltonella were almost completely depleted in two species of Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) of the Bemisia tabaci whitefly cryptic species complex. Meanwhile, proliferation of bacteriocytes was severely inhibited and approximately 50% of the nymphs had lost one of the two bacteriomes. While cell size of bacteriocytes was increased, cell number was severely decreased leading to reduction of total volume of bacteriocytes. Moreover, bacteriocyte organelles and associated symbionts were lysed, and huge amount of electron-dense inclusions accumulated. Eventually, Portiera and Hamiltonella failed to be transmitted to the next generation. In contrast, Rickettsia could be detected although at a reduced level, and successfully transmitted to eggs. The results suggest that the thermal sensitivity of bacteriocytes may limit thermal tolerance and vertical transmission of the associated symbionts, and consequently different patterns of distribution of symbionts may affect their capacity to tolerate unfavourable temperatures and persistence in the host.

Increase in temperature enriches heat tolerant taxa in Aedes aegypti midguts

“…The results of our study showed a significant dissimilarity in the midgut composition across temperature regimen. Our results are in contrast to several studies that have demonstrated a reduction in the richness of endosymbionts or complete eradication of midgut microbes in insects as a result of temperature increases [17][18][19][20] . Our studies and those studies demonstrate that temperature has an effect on gut microbes but our results may not translate to other insects sampled in other laboratories or other mosquitoes sampled in this laboratory at a different time.…”

“…The impact of temperature change on the midgut microbiome diversity of insects has mainly been studied with constant temperature. The results of such studies show a significant reduction in the richness of the midgut microbiome to complete loss of midgut microbiome as well as reduction in the vertical transmission to the next generation [17][18][19][20] . Given that temperatures fluctuate in nature; using constant temperature to study the impact of temperature on the midgut microbiome may not provide an accurate depiction.…”

Host Plant Affects Symbiont Abundance in Bemisia tabaci (Hemiptera: Aleyrodidae)

“…A new infection of S-symbionts is through occasional events of horizontal transmissions among different insect species or different individuals mediated by plant, parasitoids, or copulation [ 44 , 45 , 46 , 47 , 48 ]. High temperatures can eliminate the mutualistic partners from insect hosts; many bacteriocyte-associated symbionts have reduced densities or are lost entirely when the insect host is exposed to high temperatures [ 49 , 50 , 51 ]. Our experimental populations did not contact other infectious populations, species, or host plants fed by other infectious populations and were kept in controlled conditions in the laboratory.…”

Aphid Facultative Symbionts Aid Recovery of Their Obligate Symbiont and Their Host After Heat Stress

“…Instead of indirectly affecting the host's stress or immune responses, symbionts may themselves produce and release heat shock proteins or metabolites that directly protect the host or other microbes that the host depends on (i.e., obligate symbionts) . Obligate symbionts are often a thermal "weak link" and more susceptible to temperature extremes than their hosts (Corbin et al, 2017;Shan et al, 2017;Zhang et al, 2019). Shielding an obligate symbiont from thermal damage would therefore benefit both the host and all of its symbionts.…”