Resume

• 2019

  Rothman

  UC Irvine

  UC Irvine

• 2015

  University of California

  Riverside

• 2014

  University of California

  Riverside

  University of California

  Riverside

  Doctor of Philosophy (PhD)

  Microbiology

  University of California

  Riverside

• 2011

  California State Polytechnic University-Pomona

• 2009

  Pomona Unified School District

  California State Polytechnic University-Pomona

  Pomona Unified School District

  California State Polytechnic University-Pomona

  California State Polytechnic University-Pomona

  Master of Science (MS)

  Biological Sciences

  California State Polytechnic University-Pomona

• 2006

  Western Analytical Labs

  Western Analytical Labs

• 2005

  Bachelor of Science (BS)

  Biotechnology

  California State Polytechnic University-Pomona

• 10

  The honey bee

  Apis mellifera

  pollinates a wide variety of essential crops in numerous ecosystems around the world but faces many modern challenges. Among these

  the microsporidian pathogen Nosema ceranae is one of the primary detriments to honey bee health. Nosema infects the honey bee gut

  which harbors a highly specific

  coevolved microbiota heavily involved in bee immune function and nutrition. Here

  we extend previous work investigating interactions between the honey bee gut microbiome and N. ceranae by studying experimentally infected bees that were returned to their colonies and sampled 5

  and 21 days post-infection. We measured Nosema load with quantitative PCR and characterized microbiota with 16S rRNA gene amplicon sequencing. We found significant colony level variation in infection levels

  and subtle differences between the microbiota of colonies with high infection levels versus those with low infection levels. Two exact sequence variants of Gilliamella

  a core gut symbiont that has previously been associated with gut dysbiosis

  were significantly more abundant in bees from colonies with high Nosema loads versus those with low Nosema loads. These bacteria deserve further study to determine if they facilitate more intense infection by Nosema ceranae.

  Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure

  John T. Trumble

  Jay Gan

  Quinn S. McFrederick

  Michael B. Jones

  Marcus J. Pennington

  Drought

  rising temperatures

  and expanding human populations are increasing water demands. Many countries are extending potable water supplies by irrigating crops with wastewater. Unfortunately

  wastewater contains biologically active

  long-lived pharmaceuticals

  even after treatment. Run-off from farms and wastewater treatment plant overflows contribute high concentrations of pharmaceuticals to the environment. This study assessed the effects of common pharmaceuticals on a cosmopolitan saprophagous insect

  Megaselia scalaris (Diptera: Phoridae). Larvae were reared on artificial diets spiked with contaminants of emerging concern (CECs) at environmentally relevant concentrations. Female flies showed no oviposition preference for treated or untreated diets. Larvae exposed to caffeine in diets showed increased mortality

  and larvae fed antibiotics and hormones showed signs of slowed development

  especially in females. The normal sex ratio observed in M. scalaris from control diets was affected by exposure to caffeine and pharmaceutical mixture treatments. There was an overall effect of treatment on the flies’ microbial communities; notably

  caffeine fed insects displayed higher microbial variability. Eight bacterial families accounted for approximately 95% of the total microbes in diet and insects. Our results suggest that CECs at environmentally relevant concentrations can affect the biology and microbial communities of an insect of ecological and medical importance.

  Effects of contaminants of emerging concern on Megaselia scalaris (Lowe

  Diptera: Phoridae) and its microbial community

  Jay Kirkwood

  Laura Leger

  Honey bees are important insect pollinators used heavily in agriculture and can be found in diverse environments. Bees may encounter toxicants such as cadmium and selenate by foraging on plants growing in contaminated areas

  which can result in negative health effects. Honey bees are known to have a simple and consistent microbiome that conveys many benefits to the host

  and toxicant exposure may impact this symbiotic microbial community. We used 16s rRNA gene sequencing to assay the effects that sublethal cadmium and selenate treatments had over seven days and found that both treatments significantly but subtly altered the composition of the bee microbiome. Next

  we exposed bees to cadmium and selenate then used untargeted LC-MS metabolomics to show that chemical exposure changed the bees' metabolite profiles and that compounds which may be involved in detoxification

  proteolysis

  and lipolysis were more abundant in treatments. Lastly

  we exposed several strains of bee-associated bacteria in liquid culture and found that each strain removed cadmium from their media

  but only Lactobacillus Firm-5 microbes assimilated selenate

  indicating the possibility that these microbes may reduce metal and metalloid burden on their host. Overall

  our study shows that metal and metalloid exposure can affect the honey bee microbiome and metabolome

  and that strains of bee-associated bacteria can bioaccumulate these toxicants.

  Cadmium and selenate exposure affects the honey bee microbiome and metabolome

  and bee-associated bacteria show potential for bioaccumulation

  Quinn McFrederick

  Kirk Anderson

  William Meikle

  Mark Carroll

  Honey bees (Apis mellifera) provide vital pollination services for a variety of agricultural crops around the world and are known to host a consistent core bacterial microbiome. This symbiotic microbial community is essential to many facets of bee health

  including likely nutrient acquisition

  disease prevention and optimal physiological function. Being that the bee microbiome is likely involved in the digestion of nutrients

  we either provided or excluded honey bee colonies from supplemental floral forage before being used for almond pollination. We then used 16S rRNA gene sequencing to examine the effects of forage treatment on the bees’ microbial gut communities over four months. In agreement with previous studies

  we found that the honey bee gut microbiota is quite stable over time. Similarly

  we compared the gut communities of bees from separate colonies and sisters sampled from within the same hive over four months. Surprisingly

  we found that the gut microbial communities of individual sisters from the same colony can exhibit as much variation as bees from different colonies. Supplemental floral forage had a subtle effect on the composition of the microbiome during the month of March only

  with strains of Gilliamella apicola

  Lactobacillus

  and Bartonella being less proportionally abundant in bees exposed to forage in the winter. Collectively

  our findings show that there is unexpected longitudinal variation within the gut microbial communities of sister honey bees and that supplemental floral forage can subtly alter the microbiome of managed honey bees.

  Longitudinal Effects of Supplemental Forage on the Honey Bee (Apis mellifera) Microbiota and Inter- and Intra-Colony Variability

  Hamid M. Said

  Craig W. LaMunyon

  Daniel Elmatari

  Arundhati Biswas

  Two potential orthologs of the human riboflavin transporter 3 (hRFVT3) were identified in the C. elegans genome

  Y47D7A.16 and Y47D7A.14

  which share 33.7 and 30.5% identity

  respectively

  with hRFVT3. The genes are tandemly arranged

  and we assign them the names rft-1 (for Y47D7A.16) and rft-2 (for Y47D7A.14). Functional characterization of the coding sequences in a heterologous expression system demonstrated that both were specific riboflavin transporters

  although the rft-1 encoded protein had greater transport activity. A more detailed examination of rft-1 showed its transport of riboflavin to have an acidic pH dependence

  saturability (apparent Km = 1.4±0.5 µM)

  inhibition by riboflavin analogues

  and Na+ independence. The expression of rft-1 mRNA was relatively higher in young larvae than in adults

  and mRNA expression dropped in response to RF supplementation. Knocking down the two transporters individually via RNA interference resulted in a severe loss of fertility that was compounded in a double knockdown. Transcriptional fusions constructed with two fluorophores (rft-1::GFP

  and rft-2::mCherry) indicated that rft-1 is expressed in the intestine and a small subset of neuronal support cells along the entire length of the animal. Expression of rft-2 is localized mainly to the intestine and pharynx. We also observed a drop in the expression of the two reporters in animals that were maintained in high riboflavin levels. These results report for the first time the identification of two riboflavin transporters in C. elegans and demonstrate their expression and importance to metabolic function in worms. Absence of transporter function renders worms sterile

  making them useful in understanding human disease associated with mutations in hRFVT3.

  Identification and Functional Characterization of the Caenorhabditis elegans Riboflavin Transporters rft-1 and rft-2

  Jay Gan

  Quinn McFrederick

  Michael Jones

  Marcus Pennington

  Many countries are utilizing reclaimed wastewater for agriculture as water demands due to drought

  rising temperatures

  and expanding human populations. Unfortunately

  wastewater often contains biologically active

  pseudopersistant pharmaceuticals

  even after treatment. Runoff from agriculture and effluent from wastewater treatment plants also contribute high concentrations of pharmaceuticals to the environment. This study assessed the effects of common pharmaceuticals on an agricultural pest

  the aphid Myzus persicae (Sulzer

  Hemiptera: Aphididae). Second instar nymphs were transferred to bell peppers (Capsicum annuum) that were grown hydroponically. Treatment plants were spiked with contaminants of emerging concern (CECs) at environmentally relevant concentrations found in reclaimed wastewater. M. persicae displayed no differences in population growth or microbial community differences due to chemical treatments. Plants

  however

  displayed significant growth reduction in antibiotic and mixture treatments

  specifically in wet root masses. Antibiotic treatment masses were significantly reduced in the total and root wet masses. Mixture treatments displayed an overall reduction in plant root wet mass. Our results suggest that the use of reclaimed wastewater for crop irrigation would not affect aphid populations

  but could hinder or delay crop production.

  Effects of contaminants of emerging concern on Myzus persicae (Sulzer

  Hemiptera: Aphididae) biology and on their host plant

  Capsicum annum

  Erica Chang

  Zachary Nuetz

  Milagra Weiss

  Nicholas Brown

  Quinn McFrederick

  William Meikle

  Mark Carroll

  Supplemental forage can be used to provide nutrition to bees during winter dearth. We examined the effects of supplemental forage on colony performance

  colony survival

  worker quality

  and queen pheromone signaling in Nosema ceranae-infected overwintering colonies. Colonies were either supplemented with rapini or left unsupplemented for 1 month before almond pollination. Unsupplemented colonies experienced higher mortality than supplemented colonies. Supplemental forage did not affect colony performance

  worker mass

  or hypopharyngeal gland protein content. However

  supplemented queens released more of three queen QMP and QRP compounds (4-hydroxy-3-methoxyphenylethanol

  methyl oleate

  and 1-hexadecanol) that promote queen care among workers. In addition

  colonies that survived almond pollination thermoregulated their hives more than colonies that failed. Supplemental forage may prepare overwintering colonies for the stresses of early spring pollination.

  Pre-almond supplemental forage improves colony survival and alters queen pheromone signaling in overwintering honey bee colonies

  Diana Cox-Foster

  Corey Andrikopoulos

  Managed pollinators such as the alfalfa leafcutting bee

  Megachile rotundata

  are essential to the production of a wide variety of agricultural crops. These pollinators encounter a diverse array of microbes when foraging for food and nest-building materials on various plants. To test the hypothesis that food and nest-building source affects the composition of the bee-nest microbiome

  we exposed M. rotundata adults to treatments that varied both floral and foliar source in a 2 × 2 factorial design. We used 16S rRNA gene and internal transcribed spacer (ITS) sequencing to capture the bacterial and fungal diversity of the bee nests. We found that nest microbial communities were significantly different between treatments

  indicating that bee nests become inoculated with environmentally derived microbes. We did not find evidence of interactions between the fungi and bacteria within our samples. Furthermore

  both the bacterial and fungal communities were quite diverse and contained numerous exact sequence variants (ESVs) of known plant and bee pathogens that differed based on treatment. Our research indicates that bees deposit plant-associated microbes into their nests

  including multiple plant pathogens such as smut fungi and bacteria that cause blight and wilt. The presence of plant pathogens in larval pollen provisions highlights the potential for bee nests to act as disease reservoirs across seasons. We therefore suggest that future research should investigate the ability of bees to transmit pathogens from nest to host plant.

  Floral and foliar source affect the bee nest microbial community

  Quinn McFrederick

  Thomas Raffel

  Rodrigo Nevarez

  Lyna Ngor

  Evan Palmer-Young

  High temperatures (e.g. fever) and gut microbiota can both influence host resistance to infection. However

  effects of temperature‐driven changes in gut microbiota on resistance to parasites remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasite Crithidia bombi. Infection intensity decreased by over 80% between 21 and 37 °C. Temperatures of peak infection were lower than predicted based on parasite growth in vitro

  consistent with mismatches in thermal performance curves of hosts

  parasites

  and gut symbionts. Gut bacterial community size and composition exhibited slight but significant

  non‐linear

  and taxon‐specific responses to temperature. Abundance of total gut bacteria and of Orbaceae

  both negatively correlated with infection in previous studies

  were positively correlated with infection here. Prevalence of the bee pathogen‐containing family Enterobacteriaceae declined with temperature

  suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance

  but also temperature‐dependent activity of gut bacteria. The thermal ecology of gut parasite‐symbiont interactions may be broadly relevant to infectious disease

  both in ectothermic organisms that inhabit changing climates

  and in endotherms that exhibit fever‐based immunity.

  Temperature dependence of parasitic infection and gut bacterial communities in bumble bees

  John Trumble

  Jay Gan

  Quinn McFrederick

  Michael Jones

  Stacia Dudley

  Marcus Pennington

  Many countries are utilizing reclaimed wastewater for agriculture because drought

  rising temperatures

  and expanding human populations are increasing water demands. Unfortunately

  wastewater often contains biologically active

  pseudopersistent pharmaceuticals

  even after treatment. Runoff from farms and output from wastewater treatment plants also contribute high concentrations of pharmaceuticals to the environment. This study assessed the effects of common pharmaceuticals on an agricultural pest

  Trichoplusia ni (Lepidoptera: Noctuidae). Larvae were reared on artificial diets spiked with contaminants of emerging concern (CECs) at environmentally relevant concentrations. Trichoplusia ni showed increased developmental time and mortality when reared on artificial diets containing antibiotics

  hormones

  or a mixture of contaminants. Mortality was also increased when T. ni were reared on tomatoes grown hydroponically with the same concentrations of antibiotics. The antibiotic-treated plants translocated ciprofloxacin through their tissues to roots

  shoots

  and leaves. Microbial communities of T. ni changed substantially between developmental stages and when exposed to CECs in their diets. Our results suggest that use of reclaimed wastewater for irrigation of crops can affect the developmental biology and microbial communities of an insect of agricultural importance.

  Contaminants of emerging concern affect Trichoplusia ni growth and development on artificial diets and a key host plant

  Given limited resources for motility

  sperm cell activation must be precisely timed to ensure the greatest likelihood of fertilization. Like those of most species

  the sperm of C. elegans become active only after encountering an external signaling molecule. Activation coincides with spermiogenesis

  the final step in spermatogenesis

  when the spherical spermatid undergoes wholesale reorganization to produce a pseudopod. Here

  we describe a gene involved in sperm activation

  spe-46. This gene was identified in a suppressor screen of spe-27(it132ts)

  a sperm-expressed gene whose product functions in the transduction of the spermatid activation signal. While spe-27(it132ts) worms are sterile at 25°C

  the spe-46(hc197)I; spe-27(it132ts)IV double mutants regain partial fertility. Single nucleotide polymorphism mapping

  whole genome sequencing

  and transformation rescue were employed to identify the spe-46 coding sequence. It encodes a protein with seven predicted transmembrane domains but with no other predicted functional domains or homology outside of nematodes. Expression is limited to spermatogenic tissue

  and a transcriptional GFP fusion shows expression corresponds with the onset of the pachytene stage of meiosis. The spe-46(hc197) mutation bypasses the need for the activation signal; mutant sperm activate prematurely without an activation signal in males

  and mutant males are sterile. In an otherwise wild-type genome

  the spe-46(hc197) mutation induces a sperm defective phenotype. In addition to premature activation

  spe-46(hc197) sperm exhibit numerous defects including aneuploidy

  vacuolization

  protruding spikes

  and precocious fusion of membranous organelles. Hemizygous worms [spe-46(hc197)/mnDf111] are effectively sterile. Thus

  spe-46 appears to be involved in the regulation of spermatid activation during spermiogenesis

  with the null phenotype being an absence of functional sperm and hypomorphic phenotypes being premature spermatid activation...

  Premature Sperm Activation and Defective Spermatogenesis Caused by Loss of spe-46 Function in Caenorhabditis elegans

• University Teaching

  Local Government

  DNA Sequencing

  Bioinformatics

  Microbiology

  The bumble bee microbiome increases survival of bees exposed to selenate toxicity.

  Quinn McFrederick

  Kaleigh Russell

  Peter Graystock

  Larua Leger

  Bumble bees are important and widespread insect pollinators who face many environmental challenges. For example

  bees are exposed to the metalloid selenate when foraging on pollen and nectar from plants growing in contaminated soils. As it has been shown that the microbiome of animals reduces metalloid toxicity

  we assayed the ability of the bee microbiome to increase survivorship against selenate challenge. We exposed uninoculated or microbiota-inoculated Bombus impatiens workers to a field-realistic dose of 0.75 mg/L selenate and found that microbiota-inoculated bees survive slightly

  but significantly longer than uninoculated bees. Using 16S rRNA gene sequencing

  we found that selenate exposure altered gut microbial community composition and relative abundance of specific core bacteria. We also grew two core bumble bee microbes – Snodgrassella alvi and Lactobacillus bombicola – in selenate-spiked media and found that these bacteria grew in the tested concentrations of 0.001 mg/L to 10 mg/L selenate. Furthermore

  the genomes of these microbes harbor genes involved in selenate detoxification. The bumble bee microbiome slightly increases survivorship when the host is exposed to selenate

  but the specific mechanisms and colony-level benefits under natural settings require further study.

  The bumble bee microbiome increases survival of bees exposed to selenate toxicity.

  Quinn McFrederick

  Hoang Vuong

  Gram-stain-positive

  rod-shaped

  non-spore forming bacteria have been isolated from flowers and the guts of adult wild bees in the families Megachilidae and Halictidae. Phylogenetic analysis of the 16S rRNA gene indicated that these bacteria belong to the genus Lactobacillus

  and are most closely related to the honey-bee associated bacteria Lactobacillus kunkeei (97.0 % sequence similarity) and Lactobacillus apinorum (97.0 % sequence similarity). Phylogenetic analyses of 16S rRNA genes and six single-copy protein coding genes

  in situ and in silico DNA–DNA hybridization

  and fatty-acid profiling differentiates the newly isolated bacteria as three novel Lactobacillus species: Lactobacillus micheneri sp. nov. with the type strain Hlig3T (=DSM 104126T

  =NRRL B-65473T)

  Lactobacillus timberlakei with the type strain HV_12T (=DSM 104128T

  =NRRL B-65472T)

  and Lactobacillus quenuiae sp. nov. with the type strain HV_6T (=DSM 104127T

  =NRRL B-65474T).

  Lactobacillus micheneri sp. nov.

  Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov.

  lactic acid bacteria isolated from wild bees and flowers

  Quinn S. McFrederick

  James C. Nieh

  Kaleigh A. Russell

  Andrey Rubanov