Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity

Schmid, Martin R.; Brockmann, Axel; Pirk, Christian Walter Werner; Stanley, David; Tautz, Jürgen

doi:10.1016/j.jinsphys.2007.11.002

Cited by 140 publications

(134 citation statements)

References 32 publications

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“…This concentration is in the same magnitude as that previously calculated via the same methods for use in a PO activity assay of Tenebrio molitor (optimal found to be 4 mg mL −1 , Moret and Siva-Jothy, 2003), and used in assays of bumble bees (Korner and Schmid-Hempel, 2004) and honey bees (Schmid et al, 2008). It is not known why we were unable to produce the concentrations of 10 mM reported in Sinsabaugh et al (1991), although it is possible that heating may have aided dissolution in this case.…”

Section: Discussionsupporting

confidence: 73%

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A standardised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee, Apis mellifera

Laughton¹,

Siva‐Jothy²

2011

Apidologie

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-The prophenoloxidase activating system (ProPO-AS) is an integral part of the constitutive innate immune response in insects, the products of which are commonly assayed to assess an individual's ability to respond to immune challenges. However, there is considerable variation in the methodologies associated with these assays, and as such, it is not always clear how to interpret results. We have optimised assays for measuring phenoloxidase in its active (PO) and zymogen (ProPO) forms in the honey bee, Apis mellifera. Contrary to results for other insects, we found that the activator α-chymotrypsin, when used at a low concentration (0.5 mg mL −1 ), combined with a minimal activation time (5 min), provided optimal conditions for assaying ProPO. In addition, a saturated L-dopa solution was required for assaying both PO and ProPO. The results highlight the importance of defining the working parameters of each assay to be species-specific. honey bee / Apis mellifera / phenoloxidase / innate immunity / activator INTRODUCTIONThe innate immune system of insects consists of two broad categories of effectors: constitutive and induced (Schmid-Hempel, 2005). Constitutive responses generally comprise the humoral prophenoloxidase activating system (ProPO-AS) and cellular responses including coagulation, phagocytosis, nodule formation and encapsulation (Gillespie et al., 1997).Whilst not maintained at a constant maximum, constitutive immune responses are always present Cerenius et al., 2008), are non-specific but immediate in effect, and are responsible for clearing most of a microbial challenge very rapidly after infection (Haine et al., 2008). By contrast the induced responses, such as antimicrobial pepCorresponding author: A.M. Laughton, alice.laughton@emory.edu * Manuscript editor: Bernd Grünewald tides, occur only once the invading pathogen has been recognised. They are specific and take longer to produce, but are longer lasting in their effect (Boman and Hultmark, 1987).We concentrate on one important arm of the constitutive immune responses. The ProPO-AS is a series of complex interactions between enzymes and their zymogens, leading to the production the enzyme phenoloxidase (PO; monophenol, L-dopa:oxygen oxidoreductase, EC 1.14.18.1). PO activity ultimately results in the formation of melanin, which is subsequently involved in cuticle sclerotisation, wound healing and cellular defence responses (Mason, 1955;Ratcliffe et al., 1984;Cerenius et al., 2008). Due to the cytotoxic nature of the by-products of this process, PO is commonly stored as its inactive precursor prophenoloxidase (ProPO), and activated as part of the cascade following the recognition of foreign compounds (Ratcliffe et al., 1984;Riley, 1988; Gillespie et al., 1997; Söderhäll and Apidologie (2011) 42:1 -1

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Section: Discussionsupporting

confidence: 73%

“…The length of time that samples are incubated, both with or without a ProPO activator, prior to assaying differs between studies (Thompson, 2002;Eleftherianos et al, 2006;Schmid et al, 2008;Wilson-Rich et al, 2008). Preliminary experiments showed that PO rapidly breaks down on defrosting, even if stored on ice (unpubl.…”

Section: Activator Timecoursementioning

confidence: 99%

A standardised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee, Apis mellifera

Laughton¹,

Siva‐Jothy²

2011

Apidologie

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“…Honeybee foragers have a reduced hemocyte number in comparison to other insects and a significant decline in the capability to form nodules in response to bacterial infections (1-3, 5, 32, 34, 36-40, 45-47). Maintaining immune competence in the individual specimen, although very important, is associated with a loss of energy (34) and all these "reductions" represent a honeybee colony-level strategy with restricted hygienic behavior and highly antibacterial nest environment (6,7,35). The commercial probiotics examined in the present study obviously did not increase honeybees' fitness; on the contrary, their addition to bees' diet resulted in intestine malfunctions and created conditions favorable to development of other intestinal illnesses, such as nosemosis.…”

Section: Methodsmentioning

confidence: 99%

Impact of vertebrate probiotics on honeybee yeast microbiota and on the course of nosemosis

Ptaszyńska¹,

Borsuk²,

Mułenko³

et al. 2016

Medycyna Weterynaryjna

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The natural intestine microbiota of honeybees is dominated by Gram-negative bacteria from such families as: Enterobacteriaceae, Alcaligenaceae and Pseudomonadaceae, less numerous are Gram-positive bacteria, yeasts and other fungi. Our research was focused on the impact of commercial vertebrae probiotics, on honeybees’ intestine yeast number, hemolymph lysozyme activity and nosemosis development. The diet of honeybees was supplemented with two vertebrate probiotics recommended in beekeeping management. The former consisted of Lactobacillus casei, L. plantarum, Saccharomyces cerevisiae, and Rhodopseudomonas palustris. The latter consisted of L. acidophilus, L. delbrueckii, and Bifidobacterium bifidum. Yeasts isolated from honeybees’ intestine and detected in our research belonged to two genera: Candida and Saccharomyces. The average number of yeast Colony Forming Units (CFUs) in uninfected honeybees fed only sugar syrup was 3850 (±400.33) and after Nosema spp. infection the number rose to 19500 (±1644.40) per one honeybee. The addition of a probiotic decreased the number of detected yeast CFUs in both groups of infected and uninfected honeybees. Nosema infection did not affect lysozyme activity; therefore it was the administration of probiotics that had the main impact on the rise of lysozyme level. Most likely very vivid probiotic bacteria were treated as invaders by honeybees’ immune defense, which resulted in almost 40% rise observed in lysozyme activity. Furthermore, probiotic supplementation accelerated the nosemosis development even twofold. Probably, increased acidity of the honeybees’ intestine, which is a consequence of the uncontrolled growth of lactic acid bacteria, created conditions favorable to faster nosemosis development. Therefore, every administration of diet supplements with live microorganisms whose impact on honeybees biology and physiology is not well studied should be carried out with the greatest caution.

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“…Moreover, the constant and relatively high temperature and humidity levels maintained in a bee nest provide the perfect environment for the incubation of all kinds of microorganisms, such as protozoa, fungi, bacteria and viruses. Like all animals, individual honeybees recruit physiological and immunological defence against disease agents (Evans et al, 2006;Schmid et al, 2008;Wilson-Rich et al, 2008). Moreover, as well as individual immunity, honeybees also show several physiological, behavioural and organizational colony-level adaptations such as spatial and behavioural compartmentalization of worker bees on the nest (Naug and Camazine, 2002;Naug, 2008), social fever (Starks et al, 2000), nest construction and enrichment with antimicrobial material (Simone et al, 2009;Baracchi and Turillazzi, 2010;Baracchi et al, 2011), grooming (Kolmes, 1989;Boecking and Spivak, 1999), hygienic behaviour (Rothenbuhler and Thompson, 1956;Spivak and Gilliam, 1998a,b;Richard et al, 2008), undertaking (Visscher, 1983) and self-removing (Kralj and Fuchs, 2006;Naug and Gibbs, 2009;Rueppell et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies

Baracchi

Fadda

Turillazzi

2012

Journal of Insect Physiology

103

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a b s t r a c tSocial life is generally associated with an increased risk of disease transmission, but at the same time it allows behavioural defence at both the individual and collective level. Bees infected with deformed-wing virus were introduced into observation hives; through behavioural observations and chemical analysis of cuticular hydrocarbons from healthy and infected bees, we offer the first evidence that honeybee colonies can detect and remove infected adult bees, probably by recognising the cuticular hydrocarbon profiles of sick individuals. We also found that health-compromised colonies were less efficient at defending themselves against infected bees, thus facing an ever increasing risk of epidemics. This work reveals a new antiseptic behaviour that can only be interpreted as an adaptation at colony level and one which should be considered an element of the social immunity system of the beehive, re-enforcing the view of a colony as an integrated organism.

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Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity

Cited by 140 publications

References 32 publications

A standardised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee, Apis mellifera

A standardised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee, Apis mellifera

Impact of vertebrate probiotics on honeybee yeast microbiota and on the course of nosemosis

Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies

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