The GEP: Crowd-Sourcing Big Data Analysis with Undergraduates.

The era of 'big data' is also the era of abundant data, creating new opportunities for student-scientist research partnerships. By coordinating undergraduate efforts, the Genomics Education Partnership produces high-quality annotated data sets and analyses that could not be generated otherwise, leading to scientific publications while providing many students with research experience.

Drosophila heparan sulfate 6-O-endosulfatase Sulf1 facilitates wingless (Wg) protein degradation.

Heparan sulfate proteoglycans regulate various physiological and developmental processes through interactions with a number of protein ligands. Heparan sulfate (HS)-ligand binding depends on the amount and patterns of sulfate groups on HS, which are controlled by various HS sulfotransferases in the Golgi apparatus as well as extracellular 6-O-endosulfatases called "Sulfs." Sulfs are a family of secreted molecules that specifically remove 6-O-sulfate groups within the highly sulfated regions on HS. Vertebrate Sulfs promote Wnt signaling, whereas the only Drosophila homologue of Sulfs, Sulf1, negatively regulates Wingless (Wg) signaling. To understand the molecular mechanism for the negative regulation of Wg signaling by Sulf1, we studied the effects of Sulf1 on HS-Wg interaction and Wg stability. Sulf1 overexpression strongly inhibited the binding of Wg to Dally, a potential target heparan sulfate proteoglycan of Sulf1. This effect of Drosophila Sulf1 on the HS-Wg interaction is similar to that of vertebrate Sulfs. Using in vitro, in vivo, and ex vivo systems, we show that Sulf1 reduces extracellular Wg protein levels, at least partly by facilitating Wg degradation. In addition, expression of human Sulf1 in the Drosophila wing disc lowers the levels of extracellular Wg protein, as observed for Drosophila Sulf1. Our study demonstrates that vertebrate and Drosophila Sulfs have an intrinsically similar activity and that the function of Sulfs in the fate of Wnt/Wg ligands is context-dependent.

The role of Drosophila heparan sulfate 6-O-endosulfatase in sulfation compensation.

The biosynthesis of heparan sulfate proteoglycans is tightly regulated by multiple feedback mechanisms, which support robust developmental systems. One of the regulatory network systems controlling heparan sulfate (HS) biosynthesis is sulfation compensation. A previous study using Drosophila HS 2-O- and 6-O-sulfotransferase (Hs2st and Hs6st) mutants showed that loss of sulfation at one position is compensated by increased sulfation at other positions, supporting normal FGF signaling. Here, we show that HS sulfation compensation rescues both Decapentaplegic and Wingless signaling, suggesting a universal role of this regulatory system in multiple pathways in Drosophila. Furthermore, we identified Sulf1, extracellular HS 6-O-endosulfatase, as a novel component of HS sulfation compensation. Simultaneous loss of Hs2st and Sulf1 led to 6-O-oversulfation, leading to patterning defects, overgrowth, and lethality. These phenotypes are caused at least partly by abnormal up-regulation of Hedgehog signaling. Thus, sulfation compensation depends on the coordinated activities of Hs2st, Hs6st, and Sulf1.

A framework for leveraging network course-based undergraduate research experience (CURE) faculty to develop, validate, and administer an assessment instrument.

Over the last several years, nationally disseminated course-based undergraduate research experiences (CUREs) have emerged as an alternative to developing a novel CURE from scratch, but objective assessment of these multi-institution (network) CUREs across institutions is challenging due to differences in student populations, instructors, and fidelity of implementation. The time, money, and skills required to develop and validate a CURE-specific assessment instrument can be prohibitive. Here, we describe a co-design process for assessing a network CURE [the Prevalence of Antibiotic Resistance in the Environment (PARE)] that did not require support through external funding, was a relatively low time commitment for participating instructors, and resulted in a validated instrument that is usable across diverse PARE network institution types and implementation styles. Data collection efforts have involved over two dozen unique institutions, 42 course offerings, and over 1,300 pre-/post-matched assessment record data points. We demonstrated significant student learning gains but with small effect size in both content and science process skills after participation in the two laboratory sessions associated with the core PARE module. These results show promise for the efficacy of short-duration CUREs, an educational research area ripe for further investigation, and may support efforts to lower barriers for instructor adoption by leveraging a CURE network for developing and validating assessment tools.

A case study to engage students in the research design and ethics of high-throughput metagenomics.

Case studies present students with an opportunity to learn and apply course content through problem solving and critical thinking. Supported by the High-throughput Discovery Science & Inquiry-based Case Studies for Today's Students (HITS) Research Coordination Network, our interdisciplinary team designed, implemented, and assessed two case study modules entitled "You Are What You Eat." Collectively, the case study modules present students with an opportunity to engage in experimental research design and the ethical considerations regarding microbiome research and society. In this manuscript, we provide instructors with tools for adopting or adapting the research design and/or the ethics modules. To date, the case has been implemented using two modalities (remote and in-person) in three courses (Microbiology, Physiology, and Neuroscience), engaging over 200 undergraduate students. Our assessment data demonstrate gains in content knowledge and students' perception of learning following case study implementation. Furthermore, when reflecting on our experiences and student feedback, we identified ways in which the case study could be modified for different settings. In this way, we hope that the "You Are What You Eat" case study modules can be implemented widely by instructors to promote problem solving and critical thinking in the traditional classroom or laboratory setting when discussing next-generation sequencing and/or metagenomics research.

Making It Matter: Increasing Student-Perceived Value of Microbiology through Reflective and Critical News Story Analysis.

Even before coverage and updates on COVID-19 became a daily event in mainstream news, mass media was already full of science-focused current events stories. While relevant to our everyday lives, many popular press science articles overstate conclusions, misstate details or, at worst, purposefully spread disinformation. This iterative news analysis and writing intervention was designed to increase the visibility of real-world applications of microbiology in current events (including and beyond the 2019 coronavirus disease [COVID-19] pandemic), thereby engaging students and cultivating motivation through a positive perception of course content in accordance with expectancy-value theory. This intervention can be scaled and has been successfully used in both large- and small-enrollment microbiology classes as an active learning strategy. Students engage in science literacy at multiple levels, starting with identifying credible sources, then summarizing news articles, relating them to course content, conveying the main ideas to lay audiences, identifying in turn misleading or omitted ideas, and finally writing potential exam questions on the topic. This multifaceted analysis allows students to interact with material at many different levels in a self-directed manner as students seek out and choose articles to share with their peers. To date, anecdotal evidence suggests positive gains in student interest and perceived value of studying science.

Immune Literacy: a Call to Action for a System-Level Change.

Immune literacy-the ability to hear, learn, read, write, explain, and discuss immunological content with varied audiences-has become critically important in recent years. Yet, with its complex terminology and discipline-specific concepts, educating individuals about the immune system and its role in health and disease may seem daunting. Here, we reflect on how to demystify the discipline and increase its accessibility for a broader audience. To address this, a working group of immunology educators from diverse institutions associated with the research coordination network, ImmunoReach, convened virtually. As a result of these discussions, we request a call to action for a system-level change and present a set of practical recommendations that novice and experienced educators from diverse institutions, professional societies, and policymakers may adopt to foster immune literacy in their classrooms and communities.

Antigen and Immunogen: An Investigation into the Heterogeneity of Immunology Terminology in Learning Resources.

The need to focus on immunology education has never been greater. The coronavirus disease 2019 pandemic has revealed that a significant proportion of our society is vaccine hesitant. Some of this hesitancy may stem from a general lack of understanding of how the immune system and immunological interventions work. In addition, social media platforms undercut public health efforts by quickly propagating a multitude of misconceptions and erroneous information surrounding the science behind these interventions. The responsibility to be advocates for science is well recognized by immunology researchers, educators, and public health professionals, as evidenced by the rich body of resources developed to communicate science to the lay audience. Scientific jargon, however, can be a barrier to effective communication and can negatively impact learning and comprehension. The field of immunology is especially laden with discipline-specific terminology, which can hamper educators' efforts to convey key concepts to learners. Furthermore, a lack of consistency in accepted definitions can complicate students' conceptual understanding. Learning resources, including textbooks, published in print or available online, and exclusively digital resources, continue to serve as the primary sources of information for both educators and students. In this article, we describe a vast heterogeneity in learning resource glossary descriptions of two key conceptual terms: antigen and immunogen We provide a perspective on pedagogical strategies to address these critical terms. Using current knowledge, we recommend an approach to standardize the definitions of the terms antigen and immunogen within the immunology educator community.

Student Attitudes Contribute to the Effectiveness of a Genomics CURE.

The Genomics Education Partnership (GEP) engages students in a course-based undergraduate research experience (CURE). To better understand the student attributes that support success in this CURE, we asked students about their attitudes using previously published scales that measure epistemic beliefs about work and science, interest in science, and grit. We found, in general, that the attitudes students bring with them into the classroom contribute to two outcome measures, namely, learning as assessed by a pre- and postquiz and perceived self-reported benefits. While the GEP CURE produces positive outcomes overall, the students with more positive attitudes toward science, particularly with respect to epistemic beliefs, showed greater gains. The findings indicate the importance of a student's epistemic beliefs to achieving positive learning outcomes.

Drosophila heparan sulfate 6-O endosulfatase regulates Wingless morphogen gradient formation.

Heparan sulfate proteoglycans (HSPGs) play critical roles in the distribution and signaling of growth factors, but the molecular mechanisms regulating HSPG function are poorly understood. Here, we characterized Sulf1, which is a Drosophila member of the HS 6-O endosulfatase class of HS modifying enzymes. Our genetic and biochemical analyses show that Sulf1 acts as a novel regulator of the Wg morphogen gradient by modulating the sulfation status of HS on the cell surface in the developing wing. Sulf1 affects gradient formation by influencing the stability and distribution of Wg. We also demonstrate that expression of Sulf1 is induced by Wg signaling itself. Thus, Sulf1 participates in a feedback loop, potentially stabilizing the shape of the Wg gradient. Our study shows that the modification of HS fine structure provides a novel mechanism for the regulation of morphogen gradients.

Combating Antimicrobial Resistance Through Student-Driven Research and Environmental Surveillance.

Emerging resistance to all classes of antimicrobials is one of the defining crises of the 21st century. Many advances in modern medicine, such as routine surgeries, are predicated on sustaining patients with antimicrobials during a period when their immune systems alone cannot clear infection. The development of new antimicrobials has not kept pace with the antimicrobial resistance (AR) threat. AR bacteria have been documented in various environments, such as drinking and surface water, food, sewage, and soil, yet surveillance and sampling has largely been from infected patients. The prevalence and diversity of AR bacteria in the environment, and the risks they pose to humans are not well understood. There is consensus that environmental surveillance is an important first step in forecasting and targeting efforts to prevent spread and transmission of AR microbes. However, efforts to date have been limited. The Prevalence of Antibiotic Resistance in the Environment (PARE) is a classroom-based project that engages students around the globe in systematic environmental AR surveillance with the goal of identifying areas where prevalence is high. The format of PARE, designed as short classroom research modules, lowers common barriers for institutional participation in course-based research. PARE brings real-world microbiology into the classroom by educating students about the pressing public health issue of AR, while empowering them to be partners in the solution. In turn, the PARE project provides impactful data to inform our understanding of the spread of AR in the environment through global real-time surveillance.

Three Steps to Adapt Case Studies for Synchronous and Asynchronous Online Learning.

Pandemic SARS-CoV-2 has ushered in a renewed interest in science along with rapid changes to educational modalities. While technology provides a variety of ways to convey learning resources, the incorporation of alternate modalities can be intimidating for those designing curricula. We propose strategies to permit rapid adaptation of curricula to achieve learning in synchronous, asynchronous, or hybrid learning environments. Case studies are a way to engage students in realistic scenarios that contextualize concepts and highlight applications in the life sciences. While case studies are commonly available and adaptable to course goals, the practical considerations of how to deliver and assess cases in online and blended environments can instill panic. Here we review existing resources and our collective experiences creating, adapting, and assessing case materials across different modalities. We discuss the benefits of using case studies and provide tips for implementation. Further, we describe functional examples of a three-step process to prepare cases with defined outcomes for individual student preparation, collaborative learning, and individual student synthesis to create an inclusive learning experience, whether in a traditional or remote learning environment.

There Is More than Multiple Choice: Crowd-Sourced Assessment Tips for Online, Hybrid, and Face-to-Face Environments.

Developing effective assessments of student learning is a challenging task for faculty and even more difficult for those in emerging disciplines that lack readily available resources and standards. With the power of technology-enhanced education and accessible digital learning platforms, instructors are also looking for assessments that work in an online format. This article will be useful for all teachers, but especially for entry-level instructors, in addition to more mature instructors who are looking to become more well versed in assessment, who seek a succinct summary of assessment types to springboard the integration of new forms of assessment of student learning into their courses. In this paper, ten assessment types, all appropriate for face-to-face, blended, and online modalities, are discussed. The assessments are mapped to a set of bioinformatics core competencies with examples of how they have been used to assess student learning. Although bioinformatics is used as the focus of the assessment types, the question types are relevant to many disciplines.

Community development, implementation, and assessment of a NIBLSE bioinformatics sequence similarity learning resource.

As powerful computational tools and 'big data' transform the biological sciences, bioinformatics training is becoming necessary to prepare the next generation of life scientists. Furthermore, because the tools and resources employed in bioinformatics are constantly evolving, bioinformatics learning materials must be continuously improved. In addition, these learning materials need to move beyond today's typical step-by-step guides to promote deeper conceptual understanding by students. One of the goals of the Network for Integrating Bioinformatics into Life Sciences Education (NIBSLE) is to create, curate, disseminate, and assess appropriate open-access bioinformatics learning resources. Here we describe the evolution, integration, and assessment of a learning resource that explores essential concepts of biological sequence similarity. Pre/post student assessment data from diverse life science courses show significant learning gains. These results indicate that the learning resource is a beneficial educational product for the integration of bioinformatics across curricula.

Facilitating Growth through Frustration: Using Genomics Research in a Course-Based Undergraduate Research Experience.

A hallmark of the research experience is encountering difficulty and working through those challenges to achieve success. This ability is essential to being a successful scientist, but replicating such challenges in a teaching setting can be difficult. The Genomics Education Partnership (GEP) is a consortium of faculty who engage their students in a genomics Course-Based Undergraduate Research Experience (CURE). Students participate in genome annotation, generating gene models using multiple lines of experimental evidence. Our observations suggested that the students' learning experience is continuous and recursive, frequently beginning with frustration but eventually leading to success as they come up with defendable gene models. In order to explore our "formative frustration" hypothesis, we gathered data from faculty via a survey, and from students via both a general survey and a set of student focus groups. Upon analyzing these data, we found that all three datasets mentioned frustration and struggle, as well as learning and better understanding of the scientific process. Bioinformatics projects are particularly well suited to the process of iteration and refinement because iterations can be performed quickly and are inexpensive in both time and money. Based on these findings, we suggest that a dynamic of "formative frustration" is an important aspect for a successful CURE.

Riboflavin Riboswitch Regulation: Hands-On Learning about the Role of RNA Structures in the Control of Gene Expression in Bacteria.

American Society for Microbiology (ASM) Curriculum Guidelines highlight the importance of instruction about informational flow in organisms, including regulation of gene expression. However, foundational central dogma concepts and more advanced gene regulatory mechanisms are challenging for undergraduate biology students. To increase student comprehension of these principles, we designed an activity for upper-level biology students centered on construction and analysis of physical models of bacterial riboswitches. Students manipulate an inexpensive bag of supplies (beads, pipe cleaners) to model two conformations of a riboswitch in a bacterial transcript. After initial pilot testing, we implemented the activity in three upper-level classes at one research-intensive and two primarily undergraduate institutions. To assess student perceptions of learning gains, we utilized a pre/post-activity 5-point Likert-type survey instrument to characterize student perceptions of confidence in both their understanding of riboswitches and their ability to apply the central dogma to riboswitches. Median post-test ranks were significantly higher than median pre-test ranks (p < 0.0001) when compared by the Wilcoxon signed-rank test (n = 31). Next, we assessed post-activity knowledge via use of a rubric to score student responses on exam questions. More than 80% of students could correctly describe and diagram examples of riboswitches; data from initial iterations were used to enhance curriculum materials for subsequent implementations. We conclude that this riboswitch activity leads to both student-reported increases in confidence in the ASM curriculum dimension of gene regulation, including central dogma concepts, and demonstrated student ability to diagram riboswitches, predict outcomes of riboswitches, and connect riboswitches to evolutionary roles.

A course-based research experience: how benefits change with increased investment in instructional time.

There is widespread agreement that science, technology, engineering, and mathematics programs should provide undergraduates with research experience. Practical issues and limited resources, however, make this a challenge. We have developed a bioinformatics project that provides a course-based research experience for students at a diverse group of schools and offers the opportunity to tailor this experience to local curriculum and institution-specific student needs. We assessed both attitude and knowledge gains, looking for insights into how students respond given this wide range of curricular and institutional variables. While different approaches all appear to result in learning gains, we find that a significant investment of course time is required to enable students to show gains commensurate to a summer research experience. An alumni survey revealed that time spent on a research project is also a significant factor in the value former students assign to the experience one or more years later. We conclude: 1) implementation of a bioinformatics project within the biology curriculum provides a mechanism for successfully engaging large numbers of students in undergraduate research; 2) benefits to students are achievable at a wide variety of academic institutions; and 3) successful implementation of course-based research experiences requires significant investment of instructional time for students to gain full benefit.