Impact of a novel Rickettsia symbiont on the life history and virus transmission capacity of its host whitefly (Bemisia tabaci)

Abstract

Rickettsia consists of some of the most prevalent symbionts of insects and often plays a significant role in the biology of its hosts. Recently, a maternally inherited Torix group Rickettsia, provisionally named as RiTBt, was recorded in a species of notorious pest whitefly, tentatively named as Asia II 1, from the Bemisia tabaci complex. The role of this Rickettsia in the biology of its host is unknown. Here we investigated the impact of RiTBt on the performance and virus transmission capacity of Asia II 1. RiTBt did not significantly affect the life history parameters of the whitefly when the host insect was reared on tobacco, tomato, and cotton, three host plants with relatively low, medium and high suitability to the whitefly. Intriguingly, RiTBt slightly enhanced whitefly transmission of cotton leaf curl Multan virus (CLCuMuV), a virus that is transmitted by the whitefly in the field and has caused extensive damage to cotton production. Specifically, compared with whiteflies without RiTBt, following a 48 h virus acquisition whiteflies with RiTBt had higher titer of virus and showed higher efficiency of virus transmission. A rickettsial secretory protein BtR242 was identified as a putative virus-binding protein, and was observed to interact with the coat protein of CLCuMuV in vitro. Viral infection of the whitefly downregulated gene transcript levels of the BtR242 gene. These observations indicate that RiTBt has limited impact on the biology of the Asia II 1 whitefly, and whether this symbiont has functions in the biology of other host whiteflies warrants future investigation.

The Costs and Benefits of Two Secondary Symbionts in a Whitefly Host Shape Their Differential Prevalence in the Field

“…These phloem feeding insects have a haplodiploid genetic system in which a fertilized egg develops into a diploid female and an unfertilized egg develops into a haploid male ( Byrne and Bellows, 1991 ). The whiteflies harbor the primary symbiont “ Candidatus Portiera aleyrodidarum” (hereafter Portiera ) and seven known secondary symbionts, including Hamiltonella and Cardinium ( Zchori-Fein and Brown, 2002 ; Weeks et al, 2003 ; Gottlieb et al, 2008 ; Bing et al, 2013a , b ; Lei et al, 2021 ). In addition, these symbionts often contain some strains with genetic differentiations ( Kanakala and Ghanim, 2019 ).…”

Proteomic Analyses of Whitefly-Begomovirus Interactions Reveal the Inhibitory Role of Tumorous Imaginal Discs in Viral Retention

“…Vitellogenin may enable transovarial transmission of virus to the next generation of whitefly ( 28 ). The putative roles of Bt HSP16, thioredoxin-like protein (TLP) and protein BtR242 produced by Rickettsia in the viral transmission are yet unclear ( 29 – 31 ). Despite this progress, the functions of some of the abovementioned proteins require further validation, and many more vector components remain to be discovered to achieve an adequate understanding of begomovirus-whitefly interactions.…”

Factors Determining Transmission of Persistent Viruses by Bemisia tabaci and Emergence of New Virus–Vector Relationships

“…Retention and circulation in the hemocoel : The hemolymph of the whitefly remains the most understudied barrier, although it is thought to be a hostile environment that challenges the stability of virions. No interactions of the virus with any hemolymph proteins, hemocytes other than with the whitefly vitellogenin protein [ 44 ], or proteins secreted by the endosymbionts [ 31 , 53 , 54 , 56 ] are known ( Table 2 ). Interaction with vitellogenin is suggested to be crucial for the transovarial transmission of some begomoviruses onto oocytes [ 44 ].…”

“…Interaction with vitellogenin is suggested to be crucial for the transovarial transmission of some begomoviruses onto oocytes [ 44 ]. Direct interactions of viruses with endosymbionts scattered in the hemolymph, or indirect transmission with secreted proteins of endosymbionts localized within the bacteriosomes, have been implied to affect virus transmission in multiple studies [ 53 , 56 , 64 , 65 , 66 ]. The interaction of the GroEL protein of the bacterial symbionts with virus capsids is highlighted in its hypothesized role in the protection of virions while they circulate in the hemolymph [ 31 , 53 , 54 ] until they reach the periphery of the primary salivary glands.…”