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Published as doi: 10.1096/fj.07-101162.
 (The FASEB Journal. 2008;22:2591-2599.)
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Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies

Yuval Gottlieb*,1, Murad Ghanim*, Gwenaelle Gueguen{dagger}, Svetlana Kontsedalov*, Fabrice Vavre{dagger}, Frederic Fleury{dagger} and Einat Zchori-Fein{ddagger}

* Department of Entomology, the Agricultural Research Organization, Volcani Center, Bet-Dagan, Israel;

{dagger} UMR CNRS 5558, Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon 1, Villeurbanne, France; and

{ddagger} Department of Entomology, the Agricultural Research Organization, Newe Ya’ar Research Center, Ramat Yishay, Israel

1Correspondence: Department of Entomology, Agricultural Research Organization, Volcani Center, PO Box 6, Bet-Dagan 50250, Israel. E-mail: yuvalgd{at}yahoo.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Symbiotic relationships with bacteria are common within the Arthropoda, with interactions that substantially influence the biology of both partners. The symbionts’ spatial distribution is essential for understanding key aspects of this relationship, such as bacterial transmission, phenotype, and dynamics. In this study, fluorescence in situ hybridization was used to localize five secondary symbionts from various populations and biotypes of the sweet potato whitefly Bemisia tabaci: Hamiltonella, Arsenophonus, Cardinium, Wolbachia, and Rickettsia. All five symbionts were found to be located with the primary symbiont Portiera inside the bacteriocytes—cells specifically modified to house bacteria—but within these cells, they occupied various niches. The intrabacteriocyte distribution pattern of Rickettsia differed from what has been described previously. Cardinium and Wolbachia were found in other host tissues as well. Because all symbionts share the same cell, bacteriocytes in B. tabaci represent a unique intracellular ecosystem. This phenomenon may be a result of the direct enclosure of the bacteriocyte in the egg during oogenesis, providing a useful mechanism for efficient vertical transmission by "hitching a ride" with Portiera. On the other hand, cohabitation in the same cell provides ample opportunities for interactions among symbionts that can either facilitate (cooperation) or limit (warfare) symbiotic existence.—Gottlieb, Y., Ghanim, M., Gueguen, G., Kontsedalov, S., Vavre, F., Fleury, F., Zchori-Fein, E. Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies.


Key Words: Bemisia tabaci • fluorescent in situ hybridization • spatial distribution • vertical transmission


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
IT IS NOW WIDELY ACCEPTED that vertically transmitted microorganisms, inherited by most eukaryotes from their mothers, greatly influence a wide array of their host’s phenotypes. Some of these bacteria, the primary symbionts, are obligatory because they supplement their host’s dietary needs when the diet is nutritionally limited or unbalanced, thus directly contributing to the eukaryotic host’s fitness. These symbioses have led to intimate relationships between the two partners, as exemplified by the differentiation of specialized cells termed bacteriocytes to house the symbionts. These cells group together to form a specific organ, the bacteriome, which provides the host with a way of controlling the symbiotic population (1 , 2) . Other bacteria are facultative secondary symbionts, which may benefit host fitness under specific environmental conditions (heat stress, available host plants, or natural enemies) or manipulate the reproduction of their hosts in ways that enhance their own transmission (inducing parthenogenesis, feminizing genetic males, male-killing, and cytoplasmic incompatibility) (3 , 4) . The location of the secondary symbionts varies greatly within the host body, depending on both the bacteria and the host (e.g., ref. 5 ); localization can either be very diffuse, with invasion of the host’s entire body, leading, occasionally, to deleterious effects (6) or restricted to specific tissues, such as reproductive organs, ensuring vertical transmission (7) .

The past few years have seen a rise in the number of reported bacterial strains and species (up to six) infecting the same host species (8) . These findings illustrate the presence of symbiotic infracommunities consisting of different inherited endosymbionts with diverse effects on their hosts. Interactions in such communities may be complex, as they involve bacteriophages on top of the bacteria-bacteria relations (9) . Such multiple occurrences are widespread and probably play an important role in the evolution of symbiotic associations.

To understand the nature of symbiont infracommunities, we used confocal and electron microscopy to study the localization of symbiotic bacteria in several populations and biotypes of the sweet potato whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Portiera aleyrodidarum (Oceanospirillales), a Gammaproteobacteria, is the primary symbiont found in all whitefly species (10) . In addition, B. tabaci exhibits the highest diversity of secondary symbionts described to date, including the Gammaproteobacteria Arsenophonus (Enterobacteriales) and Hamiltonella (Enterobacteriales) (9 , 11) , Fritschea (Chlamydiales) (12) , Cardinium (Bacteroidetes) (13) , and the Alphaproteobacteria Rickettsia (Rickettsiales) (14) and Wolbachia (Rickettsiales) (15) . Of these, spatial distribution and mode of transmission have only been described for Portiera and Rickettsia (14) . Although all of these symbionts are related to bacteria that have been described from other sap-feeding insects, virtually nothing is known about their symbiont-host and symbiont-symbiont interactions.

The whitefly system presents features that make it particularly interesting for the study of symbiont localization. First, the primary symbiont Portiera is found exclusively in the bacteriocytes throughout the life cycle of its host, and the bacteriocyte itself is transmitted to each oocyte during the last stages of oogenesis (14 , 16 , 17) . During the egg and larval stages, these cells form a pair of bacteriomes, which disintegrate in the adults into cell clusters. This vertical transmission mode is unique because in other species systems, bacteria are usually transmitted directly within the egg cytoplasm (e.g., ref. 18 ). Second, secondary symbionts are usually found in secondary bacteriocytes or sheath cells, physically separated from the primary symbionts. This has been shown mainly in aphids (19 20 21) and in sharpshooters, wherein the primary symbionts are found in distinct cells (22) . Whiteflies seem to be one of the rare cases in which coinfection of primary and secondary symbionts occurs in the same cell, as shown by electron microscopy studies (17 , 23) . Third, B. tabaci is a species complex consisting of ~20 biotypes that may differ genetically and biologically (24) . Moreover, in the B and Q biotypes reported from Israel, biotype-dependent symbiotic profiles have been found (25) . The results presented in this report reveal a unique pattern of coinfection of all symbionts within the same bacteriocytes, providing one of the first detailed descriptions of what can be called an intracellular ecosystem that is inherited as a whole by the offspring.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Whitefly origin and rearing
B. tabaci individuals were sampled from field (Israel), greenhouse (France), and laboratory populations and were reared on cotton (Gossypium hirsutum ‘Acala’) under standard laboratory conditions: 26 ± 2°C, 60% relative humidity, and a photoperiod of 14:10 (light/dark). The populations studied are listed in Table 1 .


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  		Table 1. B. tabaci populations used in this study

Fluorescence in situ hybridization (FISH)
FISH of eggs, nymphs, adults, and ovaries was performed as described in Gottlieb et al. (14) , with symbiont-specific 16S/23S rRNA DNA probes (Table 2 ). Specificity of the probe sequences was tested using the Ribosomal Database Project II "probe match" analysis tool (http://rdp.cme.msu.edu/), and each probe was also aligned with all the tested sequences to reveal possible hybridization of not perfect matches. All specimens were double-stained with the Portiera-specific probe as a reference and a specific secondary symbiont probe. Stained samples were whole mounted and viewed under an IX81 Olympus FluoView 500 confocal microscope (Olympus, Tokyo, Japan). For each developmental stage, at least 100 specimens were viewed under the microscope to confirm reproducibility. Optical sections, 0.7–1.0 µm thick, were made on each specimen. Specificity of detection was confirmed using no probe staining and RNase-digested specimen staining. In addition, each population was tested with all of the probes listed in Table 2 as a control. Thus, staining of a population known not to have a symbiont but harboring others was performed.


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  		Table 2. FISH probes used for localizing bacterial symbionts in B. tabaci

Transmission electron microscopy (TEM)
Whitefly nymphs were collected from plant leaves with a fine needle into 4% (v/v) glutaraldehyde and processed using a standard method for TEM including osmification, buffer rinses, dehydration in an ascending ethanol series, propylene oxide, and embedding in Epon resin (16) . Thin sections (60–90 nm) were stained with aqueous uranyl acetate and lead citrate and examined in a Tecnai 12 electron microscope (Philips/FEI, Eindhoven, The Netherlands).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Although secondary symbionts were found located inside the bacteriocytes together with the primary symbiont at all stages of the host’s life cycle, they varied with respect to their distribution pattern. No specific signal was observed in any of the negative controls (results not shown).

Localization of Hamiltonella
Localization of Hamiltonella was studied in all populations in which it was detected by PCR (three B lines and one Q line) (Table 1) . In all individuals tested, throughout their life cycle, Hamiltonella was located in patches within the bacteriocytes among the larger-sized Portiera and was never detected in any other host organ (Figs. 1 A, 2 A, and 3 A). Colocalization of Hamiltonella and Portiera within adult bacteriocytes could also be seen in TEM (Fig. 4 A) and is suspected in nymph bacteriomes of the B. tabaci B, A, and Jatropha biotypes (17) , even though it was not strictly identified.


Figure 1
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  		Figure 1. FISH of Bemisia tabaci eggs using Portiera-specific probe (red) and probes specific to secondary symbionts. A) Hamiltonella (green); B) Arsenophonus (yellow); C) Cardinium (blue); D) Wolbachia (blue). Left column, overlay of Portiera and secondary symbiont channels; middle column, secondary symbiont channel; right column, secondary symbiont channel on brightfield channel; one optical section (A); combined optical sections (B–D).


Figure 2
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  		Figure 2. FISH of Bemisia tabaci nymphs using Portiera-specific probe (red) and probes specific to secondary symbionts. A) Hamiltonella (green); B) Arsenophonus (yellow); C) Cardinium (blue); D) Wolbachia (blue). Left column, overlay of Portiera and secondary symbiont channels; middle column, secondary symbiont channel; right column, secondary symbiont channel on brightfield channel; combined optical sections (A–D); one optical section (B, left column).


Figure 3
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  		Figure 3. FISH of Bemisia tabaci adult females using Portiera-specific probe (red) and probes specific to secondary symbionts. A) Hamiltonella (green); B) Arsenophonus (yellow); C) Cardinium (blue); D) Wolbachia (blue). Left column, secondary symbiont channel; right column, overlay of Portiera and secondary symbiont on brightfield channels; combined optical sections (A, D); one optical section (B, C).


Figure 4
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  		Figure 4. TEM sections of Bemisia tabaci. A) Portiera (P) and Hamiltonella (arrow) in adult insect’s bacteriocyte; scale bar = 4.0 µm. B) Arsenophonus (arrow) in nymph bacteriome; scale bar = 0.9 µm. N, nucleus.

Localization of Arsenophonus
Arsenophonus distribution closely resembled that of Hamiltonella. It was found restricted to the bacteriocytes in all Arsenophonus-harboring populations (Table 1) at all B. tabaci developmental stages. The highest detectable signal for this symbiont, observed as string-shaped, was found near the nuclei of the bacteriocytes (Figs. 1B , 2B , and 3B) . Moreover, TEM of Act-R nymphs revealed an Arsenophonus-like structure within the bacteriome sections (Fig. 4B ). Such intracellular localization is in agreement with light microscopy and TEM images of cell lines infected with this bacterium (26) .

Localization of Cardinium
Whereas Cardinium could be detected in the bacteriocytes throughout the life cycle of the Sigean population, it was also found outside these cells in a somewhat random distribution (Figs. 1C , 2C , and 3C) . In nymphs, higher concentrations of this bacterium were found in the abdomen and upper part of the head (Fig. 2C ). In adult females, the symbionts occupied round cells in the abdomen (suspected to be fat cells), as well as the bacteriocytes (Fig. 3C ), whereas in males they appeared to be randomly spread, excluding the rectal sac (data not shown). No Cardinium signal was detected in the thorax or head of adults. The presence of Cardinium in the bacteriocytes of B. tabaci has been demonstrated previously using TEM in the A and Jatropha biotypes (17) ; however, only the A biotype revealed both Hamiltonella and Cardinium in the same bacteriocytes together with Portiera, as shown here in the Q biotype. TEM has previously revealed the presence of Cardinium in the spermatid cytoplasm, residual bodies, and cyst cell cytoplasm of B. tabaci males (27) . Studies on other hosts have reported the presence of Cardinium in a diverse array of tissues, including the reproductive tract (28 , 29) , fat bodies, and salivary glands (30 , 31) , as well as inside bacteriocytes surrounded by oogonia in the apical region of the ovary (32) .

Localization of Wolbachia
Staining of Wolbachia produced a faint signal that was nevertheless sufficient to reveal its localization. In the eggs and nymphs of Wolbachia-positive populations (Table 1) , the bacterium was detected mostly at the circumference of and inside the bacteriocytes (Figs. 1D and 2D) . The same pattern was also seen in adult females, but in some individuals Wolbachia concentrations could also be observed in the abdomen, outside of the bacteriocytes (Fig. 3D ). The localization of Wolbachia within its arthropod hosts has been studied intensively, especially in Drosophila reproductive organs (ovaries and testes), to understand its mode of vertical transmission and its influence on host reproduction (e.g., refs. 33 34 35 ). Other studies have shown that Wolbachia is located in ovarian cells and in developing embryos (7) . However, in several insect hosts, this symbiont has been found in organs such as the salivary glands, gut structures, malpighian tubes, fat bodies, and brain (6 , 36 , 37) . Coexistence of Wolbachia with other bacterial genera has been shown in the aphid Cinara cedri, where it is found in the bacteriocytes together with Serratia symbiotica, and in the weevil Sitophilus oryzae, where it coexists with the primary symbiont (21 , 38) .

Localization of Rickettsia
The Rickettsia-specific probe was tested on individuals from Rickettsia-infected populations (Table 1) . Previously we have shown that Rickettsia in most of the developmental stages of the B. tabaci B biotype from the Ssc population is distributed throughout the whitefly’s body, excluding the bacteriocytes. The only stage at which Rickettsia can be seen in the bacteriocytes is in very young eggs: soon after the egg is laid, the Rickettsia moves out of these cells (14) . In this study, the distribution pattern of Rickettsia in other populations revealed a second phenotype: strict within-bacteriocyte localization at all developmental stages, with higher signal at the circumference (Fig. 5 ). These two phenotypes are termed, respectively, "scattered" and "confined." A scattered phenotype was found in Ssc and Msp-R populations, whereas in the AV04E and BRF populations, a proportion (60 and 30%, respectively) of the individuals observed showed the confined phenotype. In the BRI population, the phenotype of Rickettsia was confined in all individuals examined.


Figure 5
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  		Figure 5. FISH of Bemisia tabaci using Portiera-specific probe (red) and/or Rickettsia-specific probe (blue). A) egg; B) nymph. Left column, Rickettsia "confined" phenotype; right column, Rickettsia "scattered" phenotype; combined optical sections.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
B. tabaci is the species in which the highest number of secondary symbionts has been detected to date. All five secondary symbionts tested in this study were found to be located together with Portiera in the bacteriocytes at all stages of development, but whereas Arsenophonus, Hamiltonella, and confined Rickettsia phenotypes were restricted to the bacteriocytes, Wolbachia, Cardinium, and scattered Rickettsia phenotypes were also found in other tissues.

Inferring bacterial function from localization patterns
Strictly vertically transmitted symbionts must either contribute directly to host fitness or manipulate host reproduction to increase the frequency in infected females (39) . Whereas the first can be achieved with a bacteriocyte-restricted localization, manipulation of reproduction probably requires infection of reproductive organs. The highly restricted distribution patterns of Hamiltonella, Arsenophonus, and confined Rickettsia suggest that these symbionts may be involved in conferring a functional advantage to the host rather than in manipulation of reproduction. In contrast, Wolbachia, Cardinium, and scattered Rickettsia, all known to be involved in the induction of reproductive disorders in their arthropod hosts (40 41 42) , are found in the bacteriocytes at all or some developmental stages, as well as throughout the whitefly body. Thus, localization and variation of bacterial distribution in the B. tabaci body fit well with the expected effects of these bacteria as inferred from other insect hosts. Moreover, the possibility that some symbionts induce cytoplasmic incompatibility in B. tabaci has been previously suggested as a possible mechanism for biotype formation (43) .

Interestingly, Rickettsia exhibits two different localization patterns, confined and scattered. In booklice, in which Rickettsia was found to be an exclusive and obligatory symbiont, both phenotypes are found in the same individual (44) . In B. tabaci, however, the distribution pattern of Rickettsia has been found to be a stable characteristic of the symbiotic association being tested, and it is still not clear whether this phenotype results from the whitefly genotype, the bacterial genotype, or an interaction between the two. Variation in localization within a single host has been demonstrated previously for different strains of Wolbachia (35) . But whether the Rickettsia confined and scattered phenotypes are a reflection of different bacterial strains has yet to be clarified. Understanding the factors at the origin of these variations could help identify the signals involved in the targeting of specific tissues by endosymbiotic bacteria. Finally, the comparison and crossing of confined and scattered phenotypes of Rickettsia may be useful to test for reproductive disorders and their relationship with bacterial distribution within the host body.

Consequences of sharing
Here we show that although some symbionts were found throughout the B. tabaci body, all of them were present in the bacteriocytes. Colonizing a host-derived tissue that has been specially made to accommodate symbionts offers three clear advantages to the tenants. First, the bacteriocytes have a specific immune profile, allowing the host to maintain and control the symbiosis (45 , 46) . By colonizing the bacteriocytes, the symbionts are thus able to escape the host immune response; however, symbionts that are restricted to the bacteriocytes, such as Hamiltonella or Arsenophonus, might not be able to survive outside of these structures. Second, bacteriocytes are specialized for efficient, bidirectional nutrient transport between the host and its symbionts. Intrabacteriocyte localization suggests that some of these bacteria produce molecules that are important to the host. Finally, as for the primary symbiont, strict localization of the symbionts within the bacteriocytes might help keep them in low numbers so that the overall cost of bearing them is reduced.

Although coinfection of bacteriocytes by primary and secondary symbionts may not be common, this study shows that each of the five secondary symbionts tested was located together with the primary symbiont at each stage of development. It can be postulated that this phenomenon is directly related to the specific mechanism of bacteriocyte transmission during oogenesis that occurs in whiteflies. By colonizing the primary bacteriocyte, secondary symbionts do not have to individually migrate to the ovaries and enter the eggs: they simply benefit from the bacteriocyte transmission, thus hijacking the mechanism developed to transmit the primary symbiont.

On the other hand, cohabitation in the same cell undoubtedly generates constraints. First, the limited space may enhance competition among bacteria, resulting in a lower density of the primary symbiont and a potential effect on the insect’s fitness. Second, although direct antagonistic interactions such as the synthesis of antibiotics or the presence of bacteriophages are facilitated by close coexistence, theory predicts that evolution toward cooperation is possible when multiple infections are stably maintained (47) . Interestingly, some B. tabaci secondary symbionts never coexist, whereas others are frequently found together. For example, Arsenophonus and Hamiltonella have never been found together in the same individual in any of the populations tested (25) . The fact that they occupy the same niche in different biotypes of B. tabaci suggests they might have been competing in an ancestral whitefly and may provide a partial explanation for the observation that each of them can be found in a different biotype. Similarly, Rickettsia and Cardinium seem to be mutually exclusive in the same individual, and cases of Cardinium and Wolbachia in the same individual are rare (unpublished results). Our results show that the distribution of Cardinium in the whitefly’s body is similar to that of the scattered Rickettsia phenotype (14) . This finding may indicate competition outside the bacteriocyte, possibly for transmission or for movement into the bacteriocytes. Future experiments on bacterial density in symbiotic communities with different compositions should shed more light on the interactions occurring among bacterial species.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Our study revealed a unique pattern of bacteriocyte cohabitation by primary and secondary symbionts. The association of different bacterial species grouped together in the same insect cell, which establish negative or positive interactions among themselves and whose density may be regulated by the cell’s environment or other trophic levels such as bacteriophages, produces a true intracellular ecosystem that is stable throughout the life of the host and inherited from mother to offspring. The transmission of this ecosystem as a whole is ensured by the oocyte’s colonization by bacteriocytes, a phenomenon that so far has only been observed in whiteflies. Thus, one should consider an individual as a multiple-genome organism. Interestingly, recent sequencing data on secondary symbionts have demonstrated that in contrast to primary symbionts, their genomes are highly dynamic, prone to recombination, and frequently invaded by mobile elements such as insertion sequences and bacteriophages. Moreover, genetic exchange among endosymbionts is suggested to occur (reviewed in ref. 48 ). The inherited intracellular ecosystem in B. tabaci provides ample opportunities for such dynamics. Coinfections also raise the possibility of direct antagonistic or cooperative interactions among partners that could be manipulated to develop alternative methods of pest control using the symbiotic diversity of whiteflies. In fact, symbiotic bacteria are directly involved in the transmission of viruses through whitefly vectors (49) , and the ability to transmit viruses may vary according to the symbiotic complement. Clearly, sequencing the genomes of these symbionts could shed light on numerous characteristics through evolutionary and functional genomics studies.


   ACKNOWLEDGMENTS
 
This research was supported by the High Council for Scientific and Technological Cooperation between France and Israel and the program on sustainable agriculture (CNOUS 05F14). This work was also supported by the Agence Nationale de la Recherche/The French National Research Agency under the Programme Agriculture et Développement Durable (project ANR-06-PADD-04, BemisiaRisk). The authors gratefully acknowledge the help of Rami Horowitz and Henryk Czosnek in collecting and maintaining the whitefly populations. Thanks are extended to Abdelaziz Heddi for helpful discussions. The authors also thank Eddy Belausov and Luciano Sacchi for their technical help. This is Contribution 509/07 from the Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel.

Received for publication November 22, 2007. Accepted for publication January 10, 2008.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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