Snodgrassella alvi

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Snodgrassella alvi
Snodgrassella alvi EM Kwong.jpg
Snodgrassella alvi, electron micrograph
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Pseudomonadota
Class: Betaproteobacteria
Order: Neisseriales
Family: Neisseriaceae
Genus: Snodgrassella
Species:
S. alvi
Binomial name
Snodgrassella alvi
Kwong and Moran 2013

Snodgrassella alvi is a species of Gram-negative bacteria within the Neisseriaceae and was previously the only known species of the genus Snodgrassella. It was isolated and scientifically described in 2012 by Waldan K. Kwong and Nancy A. Moran, who named the bacteria after the American entomologist Robert Evans Snodgrass.

Snodgrassella alvi lives symbiotically as part of the intestinal flora in the midgut of honeybees (Apis mellifera) and some social bumblebee species. In this section of the intestine, together with Gilliamella apicola , they are the dominant bacteria, with each representing up to nearly 40% of the microflora there. In the intestine, Snodgrassella alvi and Gilliamella apicola interact in the utilization of metabolic resources, using each other's metabolites, and accordingly, they colonize different areas of the intestinal wall.

According to a study published in September 2018, Snodgrassella alvi is damaged by the use of the pesticide glyphosate, resulting in impairments of the gut microbiota. As a result, weakening of the bees' resistance to harmful bacteria and subsequent weakening of the animals was observed. [1] This effect was subsequently discussed internationally in various media as a possible cause of the colony collapse disorder observed worldwide.

Characteristics

Appearance

Snodgrassella alvi is a bacterial species and thus a unicellular organism without a nucleus (prokaryote). The individual cells are short and rod-shaped with a length of about 1.0 µm and a diameter of 0.4 µm. They are gram-negative and accordingly possess only a thin peptidoglycan envelope. [2]

Colonies of Snodgrassella alvi on blood agar Snodgrassella alvi Blutagar Kwong 01.jpg
Colonies of Snodgrassella alvi on blood agar

The bacteria are immobile and form colonies with other bacteria in the bays of the intestinal wall of the bee gut. The strains can grow on blood agar, trypticase soy agar (TSA), heart infusion agar (HIA), and lysogeny broth (LB), forming smooth, white, and round colonies about 1 millimeter or less in diameter after 2 days. [2]

Growth and metabolism

The species is microaerophilic, i.e. grows best at low oxygen levels. A five percent CO2 atmosphere at a temperature of 37 °C provides optimal growth conditions, while the bacteria show very weak or no growth in air or without oxygen (anaerobic). In the TSA, the growth range is approximately pH 6.0 to 6.5. [2] The catalase test and the test for nitrate reductases are positive, while the oxidase test (detection of the enzyme cytochrome c oxidase) is negative. Tests of the strains for β-glucosidase, β-galactosidase, indole production, proteolysis of gelatin, and glucose fermentation are negative. They are not hemolytic and show variable reactions to urease and arginine dihydrolase. [2]

The bacterium can use citric and malic acid as its main carbon source. [2]

Chemotaxonomic features

The combined content of cytosine and guanine (GC-content) in DNA is 41 to 43 mol%. The main isoprenoid quinone is ubiquinone-10. The main components of the fatty acids produced are palmitic acid (C 16:0), cis-vaccenic acid (C 18:1ω7 c/C 18:1ω6 c) and lauric acid (C 12:0), [2] by which Snodgrassella alvi can be distinguished from closely related species. [3]

Genome

The genome of Snodgrassella alvi has been completely sequenced. [4] [5] Out of 2,226 protein-coding genes, 519 genes are essential and 399 genes are involved in gut colonization of honeybees. [6]

Lifestyle and physiology

Apis mellifera Western honey bee.jpg
Bee anatomy.jpg
Snodgrassella alvi lives in the gut of honey bees. Together with Gilliamella apicola, it dominates the ileum area (k) behind the midgut (i) and the pylorus (l)

Snodgrassella alvi lives in the gut of honey bees and other corbiculate (pollen-basket) bees. Strains comparable in genome were found in all subsequently studied species of the genera Apis (n=6) and Bombus (n=8) and in 9 out of 13 studied species of stingless bees (Meliponini); [7] it is not detected in other species and outside their hosts. It is a keystone species in the honeybee gut and dominates this microbiome together with seven other species, some of which have not yet been finally identified: Lactobacillus spp. Firm-4, Lactobacillus spp. Firm-5 (phylum Firmicutes), Bifidobacterium spp. (phylum Actinobacteria), Gilliamella apicola, Frischella perrara , Bartonella apis , and Alpha 2.1 (phylum Proteobacteria). Together, these species represent 95% of the intestinal bacteria. Snodgrassella alvi, Gilliamella apicola, and Frischella perrara are considered species-specific keystone species. [8]

Snodgrassella alvi and the gammaproteobacterium Gilliamella apicola dominate the area of the ileum and colonize the inner wall of the intestine there. Only a few bacteria exist in the anterior region of the intestine, while Frischella perrara dominates the short region of the pylorus and is found almost exclusively there. In the rectum, Lactobacillus strains and Bifidobacterium are predominant. [9]

The transmission of the microbiome and especially of key species occurs in social insects within the hive via the transmission of saliva and food. Bee larvae and young workers are almost devoid of gut bacteria in their first days of life and acquire their normal gut microbial flora orally only later through social interactions with other workers and by transmission between individuals within a hive during mutual food transfer (trophallaxis) in their first days outside the combs and at the beginning of their life in the colony. [10] [8] [1] Although larvae are also fed by workers, their intestines, whose anterior and posterior parts are not connected before pupation, are almost free of bacteria. This is mainly attributed to a strong immune defense of the larvae and a bacteriocidal effect of the saliva of the feeding bees. [10] Only after pupation and in the presence of nurse bees or the feces of these bees do the young workers develop the intestinal flora typical of the hive. In contrast, when exposed only to the hive material such as honeycomb, honey and bee bread or only to the saliva of bees and trophallaxis of other bees, they form atypical intestinal flora. [8]

Within the intestine, the bacteria support the digestion of honey and pollen and probably also have a function in the immune defense against parasites and pathogenic bacteria. [11] The protective effect of the natural bacterial composition has been demonstrated, among other things, against pathogens such as the protozoa Crithidia bombi or Nosema bombi , which infect various bumblebee species and lead to potentially fatal infections. [12] [13] However, excessive colonization of the bee gut by Snodgrassella alvi is likely to disrupt the gut flora and increase susceptibility to infection by the trypanosome Lotmaria passim . [14]

Interaction with Gilliamella apicola

Interactions in metabolism between Gilliamella apicola and Snodgrassella alvi (simplified). Bacterial interaction honey bee gut 01.gif
Interactions in metabolism between Gilliamella apicola and Snodgrassella alvi (simplified).

Within the bee gut, the two dominant species Gilliamella apicola and Snodgrassella alvi occupy different areas of the gut and different metabolic niches. Together, they form a biofilm on the inner gut wall, where the colonies of Snodgrassella alvi sit directly on the gut wall and the colonies of Gilliamella apicola cover them. [4] [15] [16]

Gilliamella apicola is a bacterium that breaks down sugars and produces carboxylic acids (saccharolytic fermenter), while Snodgrassella alvi oxidizes carboxylic acids. In the gut, they form a metabolic resource-sharing network in which each species benefits from the properties of the other. Gilliamella apicola appropriately converts simple carbohydrates (sugars) into energy through glycolysis and passes the leftover molecules to Snodgrassella alvi, which has and uses the genes necessary for the Krebs cycle but cannot perform glycolysis. Both species also have numerous genes and proteins that enable intestinal colonization and interactions between bacterial cells. [4]

Variations in these genes could explain the host fidelity of the strains observed in previous phylogenetic studies. Strains of Snodgrassella alvi can colonize their ancestral bee host but not bees of another genus. [4] Consistent with specific, long-term host association, comparative genomic analysis revealed major differences and little or no gene flow between gut symbionts of bumblebees and bees. However, within a host type (Apis or Bombus), researchers detected evidence of horizontal gene transfer between Gilliamella apicola and Snodgrassella alvi, demonstrating the importance of the broader gut community in directing the evolution of individual members. The results indicated that host specificity is likely influenced by several factors, including direct interactions of bacteria with hosts, microbe-microbe interactions, and social transmission of gut flora. [4]

Effect of antibiotics and glyphosate

The effects of various substances on the intestinal flora of bees have only been selectively researched. There are studies on the effect of antibiotics and glyphosate on the bacterial flora and especially on the colonization by Gilliamella apicola and Snodgrassella alvi.

In 2017, Kasie Raymann and colleagues studied the effect of the antibiotic tetracycline, which is used in hives in part to prevent bacterial infections of bee larvae, on the intestinal flora of bees. They found that the treatment led to a reduction in the number of cells of Snodgrassella alvi, while Gilliamella apicola was hardly reduced in number. [17] However, in a second study, they found that there was a shift in genotypes in Gilliamella apicola in favor of antibiotic-resistant cells, resulting in a reduction in genetic diversity, while genetic diversity in Snodgrassella alvi was not affected. [16] According to their studies, antibiotic exposure also resulted in reduced survival of bees, both in the hive and in laboratory experiments in which the bees were exposed to opportunistic bacterial pathogens. [17]

It is generally assumed that the herbicide glyphosate is harmless to animals, including bees and other insects, because its action targets the enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), which is found only in plants and microorganisms. However, when making this assumption the effects of glyphosate on animal microbiomes had not been considered, including the microorganisms that colonize the bee gut,. The gene encoding EPSPS is present in almost all sequenced genomes of bee gut bacteria, suggesting that they are potentially susceptible to glyphosate. According to a study published in September 2018, glyphosate affects the gut microbiota of young honey bees by inhibiting the shikimate pathway, particularly in Snodgrassella alvi. Exposure of bees to glyphosate thus alters, at least experimentally, the gut microbiota of young honeybee workers, thereby also increasing the bees' susceptibility to infection. As a result, a weakening of resistance to opportunistic pathogens and especially the harmful bacterial species Serratia marcescens has been observed, which is associated with increased mortality in the bees. [1] This effect has been discussed in the press as a possible cause of the colony collapse disorder observed internationally. [18] [19] [20] [21] However, resistance of some strains of Snodgrassella alvi to glyphosate has also been described. [1]

Use for mite repellent and infection control

Varroa mite on a bee in a scanning electron microscope Varroa destructor on honeybee host.jpg
Varroa mite on a bee in a scanning electron microscope

In January 2020, the results of a research project were published in which genetically modified Snodgrassella alvi were used to strengthen the bees' immune defenses against infestation by the varroa mite (Varroa destructor) and virus infections induced by it. [22] The team modified the bacteria to produce labeled double-stranded RNA (dsRNA) through an incorporated plasmid. The dsRNA module can be targeted to interfere with specific bee genes as well as key virus and mite genes. In the laboratory, gene expression of the selected region could be blocked for at least 15 days when the modified bacteria established in the bee gut and continuously expressed the dsRNA. As an effect, the survival of varroa mites on the bees was reduced as well as the transmission and infection with deformed wing virus was inhibited. [22]

Taxonomy

External systematics

Snodgrassella alvi was isolated from the gut of the European honey bee by Waldan K. Kwong and Nancy A. Moran together with Gilliamella apicola and described scientifically in 2012. Even before that, both species were identified by Vincent G. Martinson and colleagues also in the research group of Nancy A. Moran, and provisionally named as Candidatus Snodgrassella alvi and Gilliamella apicola. [10] The genus Snodgrassella was named after the American entomologist Robert Evans Snodgrass, honoring him as a pioneer in the study of insect physiology in the early 20th century, while the species epithet "alvi" refers to the lacunae of the bee intestine. [2] The type strain is wkB2 T (= NCIMB 14803 T = ATCC BAA-2449 T = NRRL B-59751 T), [23] isolated from the gut of the western honeybee (A. mellifera) in Connecticut.

Phylogenetic position of Snodgrassella alvi according to Kwong 2017. [24]

The bacteria are classified as Betaproteobacteria within the Neisseriaceae and are related to similar bacteria found in the gut of termites or other insects. [2] [4] Kwong created a cladogram of the Neisseriaceae in 2017 based on published genomic data, in which he placed Snodgrassella alvi as a sister species to Stenoxybacter acetivorans, a species found in the intestines of termites, and placed it at the base of a taxon consisting of the genera Neisseria (polyphyletic), Eikenella, Conchiformibius, Alysiella, Simonsiella, Klingella, and Bergeriella, along with the genus Vitreoscilla. [25] While the more basal taxa are found primarily in open habitats such as soil or aquatic environments, the derived forms including Stenoxybacter and Snodgrassella are generally attached to other organisms, primarily animals. [24]

A research group led by Chinese researcher Yong Li grouped Vitreoscilla, Stenoxybacter, and Snodgrassella into a taxon that additionally includes the species Populibacter corticis, newly described in the paper, from the bark of a Canadian poplar (Populus × euramericana) canker as a sister species of Snodgrassella alvi. [3]

Strains and host specificity

Within the species, bacteria are classified according to strains taken from different hosts. Accordingly, the strain wkB2 T used for the initial description was isolated from the gut of the Western honeybee (Apis mellifera) in Connecticut. As a specialized gut symbiont, Snodgrassella alvi evolved for millions of years with honeybees and bumblebees (genus Bombus), where the bacteria are found.

Investigations revealed that the different strains of Snodgrassella alvi from honey bees worldwide hardly differ in the gene sequences of the 16S rRNA (in the V4 region) and are almost identical. In contrast, there are differences in the single-copy gene minD (an ATPase that inhibits cell division) mainly in strains of Snodgrassella alvi from honeybees, while bumblebees have only one strain of Snodgrassella alvi. [26] When comparing Snodgrassella alvi strains from honey bees with those from different bumblebee species, it was found that genetic variability within individual honey bees of a hive is significantly higher than among bumblebees of a colony, the diversity being attributed to the establishment of a bee colony by swarms of workers as opposed to a single bumblebee. [26] As a result, the gut of individual honeybees is usually colonized (86%) by multiple strains of Snodgrassella alvi, whereas that of bumblebees usually contains only one strain (72%). In addition, host specificity of honey bee bacteria was found, with no strains found in both honey bee and bumblebee species. Within bumblebees, there are some Snodgrassella alvi strains that are species- or subgenus-specific, while others are found in multiple species of different subgenera. [26] Further analysis revealed that there are significantly greater differences in the protein-coding genes of honeybee strains of Snodgrassella alvi, in contrast to those of rRNA. This is explained by the fact that the variability of the 16S rRNA loci had been restricted by frequent recombination within populations, while other regions of the genome continuously evolve and diversify in adaptation to changing ecological conditions in the gut. [27]

Related Research Articles

<span class="mw-page-title-main">Bee</span> Clade of insects

Bees are winged insects closely related to wasps and ants, known for their roles in pollination and, in the case of the best-known bee species, the western honey bee, for producing honey. Bees are a monophyletic lineage within the superfamily Apoidea. They are currently considered a clade, called Anthophila. There are over 20,000 known species of bees in seven recognized biological families. Some species – including honey bees, bumblebees, and stingless bees – live socially in colonies while most species (>90%) – including mason bees, carpenter bees, leafcutter bees, and sweat bees – are solitary.

<span class="mw-page-title-main">Bacteroidota</span> Phylum of Gram-negative bacteria

The phylum Bacteroidota is composed of three large classes of Gram-negative, nonsporeforming, anaerobic or aerobic, and rod-shaped bacteria that are widely distributed in the environment, including in soil, sediments, and sea water, as well as in the guts and on the skin of animals.

<span class="mw-page-title-main">Gut microbiota</span> Community of microorganisms in the gut

Gut microbiota, gut microbiome, or gut flora are the microorganisms, including bacteria, archaea, fungi, and viruses, that live in the digestive tracts of animals. The gastrointestinal metagenome is the aggregate of all the genomes of the gut microbiota. The gut is the main location of the human microbiome. The gut microbiota has broad impacts, including effects on colonization, resistance to pathogens, maintaining the intestinal epithelium, metabolizing dietary and pharmaceutical compounds, controlling immune function, and even behavior through the gut–brain axis.

<i>Bacteroides</i> Genus of bacteria

Bacteroides is a genus of Gram-negative, obligate anaerobic bacteria. Bacteroides species are non endospore-forming bacilli, and may be either motile or nonmotile, depending on the species. The DNA base composition is 40–48% GC. Unusual in bacterial organisms, Bacteroides membranes contain sphingolipids. They also contain meso-diaminopimelic acid in their peptidoglycan layer.

<i>Bacteroides fragilis</i> Species of bacterium

Bacteroides fragilis is an anaerobic, Gram-negative, pleomorphic to rod-shaped bacterium. It is part of the normal microbiota of the human colon and is generally commensal, but can cause infection if displaced into the bloodstream or surrounding tissue following surgery, disease, or trauma.

<span class="mw-page-title-main">Microbial symbiosis and immunity</span>

Long-term close-knit interactions between symbiotic microbes and their host can alter host immune system responses to other microorganisms, including pathogens, and are required to maintain proper homeostasis. The immune system is a host defense system consisting of anatomical physical barriers as well as physiological and cellular responses, which protect the host against harmful microorganisms while limiting host responses to harmless symbionts. Humans are home to 1013 to 1014 bacteria, roughly equivalent to the number of human cells, and while these bacteria can be pathogenic to their host most of them are mutually beneficial to both the host and bacteria.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, mutualistic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

Two-spotted bumble bee Species of bee

The two-spotted bumble bee is a species of social bumble bee found in the eastern half of the United States and the adjacent south-eastern part of Canada. In older literature this bee is often referred to as Bremus bimaculatus, Bremus being a synonym for Bombus. The bee's common name comes from the two yellow spots on its abdomen. Unlike many of the other species of bee in the genus Bombus,B. bimaculatus is not on the decline, but instead is very stable. They are abundant pollinators that forage at a variety of plants.

Nancy A. Moran is an American evolutionary biologist and entomologist, University of Texas Leslie Surginer Endowed Professor, and co-founder of the Yale Microbial Diversity Institute. Since 2005, she has been a member of the United States National Academy of Sciences. Her seminal research has focused on the pea aphid, Acyrthosiphon pisum and its bacterial symbionts including Buchnera (bacterium). In 2013, she returned to the University of Texas at Austin, where she continues to conduct research on bacterial symbionts in aphids, bees, and other insect species. She has also expanded the scale of her research to bacterial evolution as a whole. She believes that a good understanding of genetic drift and random chance could prevent misunderstandings surrounding evolution. Her current research goal focuses on complexity in life-histories and symbiosis between hosts and microbes, including the microbiota of insects.

<i>Bifidobacterium longum</i> Species of bacterium

Bifidobacterium longum is a Gram-positive, catalase-negative, rod-shaped bacterium present in the human gastrointestinal tract and one of the 32 species that belong to the genus Bifidobacterium. It is a microaerotolerant anaerobe and considered to be one of the earliest colonizers of the gastrointestinal tract of infants. When grown on general anaerobic medium, B. longum forms white, glossy colonies with a convex shape. B. longum is one of the most common bifidobacteria present in the gastrointestinal tracts of both children and adults. B. longum is non-pathogenic, is often added to food products, and its production of lactic acid is believed to prevent growth of pathogenic organisms.

<i>Akkermansia muciniphila</i> Species of bacterium

Akkermansia muciniphila is a human intestinal symbiont, isolated from human feces. It is a mucin-degrading bacterium belonging to the genus, Akkermansia, discovered in 2004 by Muriel Derrien and Willem de Vos at Wageningen University of the Netherlands. It belongs to the phylum Verrucomicrobiota and its type strain is MucT. It is under preliminary research for its potential association with metabolic disorders.

The altered Schaedler flora (ASF) is a community of eight bacterial species: two lactobacilli, one Bacteroides, one spiral bacterium of the Flexistipes genus, and four extremely oxygen sensitive (EOS) fusiform-shaped species. The bacteria are selected for their dominance and persistence in the normal microflora of mice, and for their ability to be isolated and grown in laboratory settings. Germ-free animals, mainly mice, are colonized with ASF for the purpose of studying the gastrointestinal (GI) tract. Intestinal mutualistic bacteria play an important role in affecting gene expression of the GI tract, immune responses, nutrient absorption, and pathogen resistance. The standardized microbial cocktail enabled the controlled study of microbe and host interactions, role of microbes, pathogen effects, and intestinal immunity and disease association, such as cancer, inflammatory bowel disease, diabetes, and other inflammatory or autoimmune diseases. Also, compared to germfree animals, ASF mice have fully developed immune system, resistance to opportunistic pathogens, and normal GI function and health, and are a great representation of normal mice.

Apicystis bombi is a species of parasitic alveolates in the phylum Apicomplexa. It infects bees, especially bumblebees. It is believed to have a cosmopolitan distribution in bumblebees and a sporadic occurrence in honey bees, and causes disease symptoms in nonresistant bee species.

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Bartonella apis is a bacterium from the genus Bartonella. Bartonella apis was first isolated from the gut of the honey bee in 2015 by Swiss researchers at the University of Lausanne. To date, it has been found only as a gut symbiont of honey bees, including the Western honey bee, and the Eastern or Asiatic honey bee.

Mucispirillum is a genus in the phylum Deferribacterota (Bacteria). It is represented by the single species Mucispirillum schaedleri|. It has been found in the intestinal tract of some rodents and considered a commensal with some association to disease. This species has been found in cockroaches mice, turkeys, dogs, pigs, goats, termites, and sometimes humans. It is anaerobic and does not form spores. It is motile, flagellated and thought to have the ability to move through mucus.

<i>Bacteroides thetaiotaomicron</i> Species of bacterium

Bacteroides thetaiotaomicron is a gram-negative, rod shaped obligate anaerobic bacterium that is a prominent member of the normal gut microbiome in the distal intestines. Its proteome, consisting of 4,779 members, includes a system for obtaining and breaking down dietary polysaccharides that would otherwise be difficult to digest. B. thetaiotaomicron is also an opportunistic pathogen, meaning it may become virulent in immunocompromised individuals. It is often used in research as a model organism for functional studies of the human microbiota.

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Apibacter is a genus of bacteria from the family of Weeksellaceae.

Apibacter adventoris is a mesophilic bacterium from the genus of Apibacter which has been isolated from honey bees.

References

  1. 1 2 3 4 Erick V. S. Motta, Kasie Raymann, Nancy A. Moran: Glyphosate perturbs the gut microbiota of honey bees. In: Proceedings of the National Academy of Sciences 115 (41), 2018; S. 10305–10310. doi : 10.1073/pnas.1803880115.
  2. 1 2 3 4 5 6 7 8 Waldan K. Kwong, Nancy A. Moran: Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order 'Enterobacteriales' of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology, Band 63, 6, 5. Oktober 2012, doi : 10.1099/IJS.0.044875-0.
  3. 1 2 Yong Li, Han Xue, Sheng-qi Sang, Cai-li Lin, Xi-zhuo Wang: Phylogenetic analysis of family Neisseriaceae based on genome sequences and description of Populibacter corticis gen. nov., sp. nov., a member of the family Neisseriaceae, isolated from symptomatic bark of Populus × euramericana canker. PLOS ONE, 13. April 2017. doi : 10.1371/journal.pone.0174506.
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  11. ↑ P. Engel, Nancy A. Moran: The gut microbiota of insects – diversity in structure and function. In: FEMS Microbiology Reviews, 37(5), 699–735, 1. September 2013. doi : 10.1111/1574-6976.12025.
  12. ↑ Koch, Hauke; Schmid-Hempel, Paul (2011-11-29). "Socially transmitted gut microbiota protect bumble bees against an intestinal parasite". Proceedings of the National Academy of Sciences. 108 (48): 19288–19292. Bibcode:2011PNAS..10819288K. doi: 10.1073/pnas.1110474108 . ISSN   0027-8424. PMC   3228419 . PMID   22084077.
  13. ↑ Daniel P. Cariveau, J. Elijah Powell, Hauke Koch, Rachael Winfree, Nancy A. Moran: Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). The ISME Journal 8, 2014; S. 2369–2379. doi : 10.1038/ismej.2014.68.
  14. ↑ R. S. Schwarz, N. A. Moran, J. D. Evans: Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. In: Proceedings of the National Academy of Sciences. Band 113, Nummer 33, 08 2016, S. 9345–9350, doi : 10.1073/pnas.1606631113, PMID 27482088, PMC   4995961.
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  21. ↑ Baier, Tina. "Insektensterben: Macht Glyphosat die Bienen krank?". Süddeutsche Zeitung (in German). Retrieved 2022-08-17.
  22. 1 2 Sean P. Leonard, J. Elijah Powell, Jiri Perutka, Peng Geng, Luke C. Heckmann, Richard D. Horak, Bryan W. Davies, Andrew D. Ellington, Jeffrey E. Barrick, Nancy A. Moran: Engineered symbionts activate honey bee immunity and limit pathogens. Science 367 (6477), 31. Januar 2020; S. 573–576. doi : 10.1126/science.aax9039.
  23. ↑ W. K. Kwong, N. A. Moran: Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order 'Enterobacteriales' of the Gammaproteobacteria. In: International journal of systematic and evolutionary microbiology. Band 63, Pt 6Juni 2013, S. 2008–2018, doi : 10.1099/ijs.0.044875-0, PMID 23041637.
  24. 1 2 Kwong, Waldan K. (2017-05-13). "Whole genome phylogeny of Neisseriaceae species". wkkwong.com. Archived from the original on 2017-11-27. Retrieved 2022-08-17.
  25. ↑ Waldantgu K. Kwong, Hao Zheng, Nancy A. Moran: Convergent evolution of a modified, acetate-driven TCA cycle in bacteria. Nature Microbiology 2, 2017; Artikel 17067. doi : 10.1038/nmicrobiol.2017.67.
  26. 1 2 3 Elijah Powell, Nalin Ratnayeke Nancy A. Moran: Strain diversity and host specificity in a specialized gut symbiont of honeybees and bumblebees. Molecular Ecology 25 (18), September 2016; S. 4461–4471. doi : 10.1111/mec.13787.
  27. ↑ Philipp Engel, Ramunas Stepanauskas, Nancy A. Moran: Hidden Diversity in Honey Bee Gut Symbionts Detected by Single-Cell Genomics. PLOS Genetics, 11. September 2014. doi : 10.1371/journal.pgen.1004596.

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