10
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Barriers to integration of bioinformatics into undergraduate life sciences education: A national study of US life sciences faculty uncover significant barriers to integrating bioinformatics into undergraduate instruction

      research-article
      1 , 2 , 3 , 4 , 5 , 6 , 2 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 26 , 27 , 28 , *
      PLoS ONE
      Public Library of Science

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Bioinformatics, a discipline that combines aspects of biology, statistics, mathematics, and computer science, is becoming increasingly important for biological research. However, bioinformatics instruction is not yet generally integrated into undergraduate life sciences curricula. To understand why we studied how bioinformatics is being included in biology education in the US by conducting a nationwide survey of faculty at two- and four-year institutions. The survey asked several open-ended questions that probed barriers to integration, the answers to which were analyzed using a mixed-methods approach. The barrier most frequently reported by the 1,260 respondents was lack of faculty expertise/training, but other deterrents—lack of student interest, overly-full curricula, and lack of student preparation—were also common. Interestingly, the barriers faculty face depended strongly on whether they are members of an underrepresented group and on the Carnegie Classification of their home institution. We were surprised to discover that the cohort of faculty who were awarded their terminal degree most recently reported the most preparation in bioinformatics but teach it at the lowest rate.

          Related collections

          Most cited references39

          • Record: found
          • Abstract: not found
          • Article: not found

          Biology: The big challenges of big data.

            Bookmark
            • Record: found
            • Abstract: found
            • Article: found
            Is Open Access

            A Broadly Implementable Research Course in Phage Discovery and Genomics for First-Year Undergraduate Students

            INTRODUCTION In 2012, the President’s Council of Advisors on Science and Technology (PCAST) reported that there is a need for an additional one million science, technology, engineering, and mathematics (STEM) graduates in the United States over the next decade to meet U.S. economic demands (1). It was noted that even a modest increase in the persistence of STEM students in the first 2 years of their undergraduate education would alleviate much of this shortfall (1). Replacing conventional introductory laboratory courses with discovery-based research courses is a key recommendation that is expected to lead to enhanced retention. Providing authentic research experiences to undergraduate students and directing them toward careers in STEM is a priority of science education in the 21st century (1 – 4). An abundance of evidence shows that involvement of undergraduate students in authentic research experiences has strong benefits for their engagement and interest in science (5 – 7) and that this often increases student interest in STEM careers (8). It is common for undergraduate students at research colleges and universities to participate in faculty-led research programs—especially during their last 2 years—with graduate students and postdoctoral researchers participating in their mentorship (9). Research experiences promote college retention (10), but the capacity for high-quality mentored undergraduate research within faculty research programs is limited, and this route is unlikely alone to satisfy the economic demands of the coming decade. There have been many successful efforts to develop classroom undergraduate research experiences (11–14; see also http://www.sciencemag.org/site/special/ibi/ and http://www.curenet.org/), but identifying authentic research experiences that scale to larger numbers of undergraduate students often proves elusive (4). Bioinformatic approaches engaging substantial numbers of students at diverse institutions have been described (15, 16) and are successful in providing research experiences (14) but do not include a wet-bench laboratory component. Taking advantage of research infrastructures at research-intensive institutions to advance missions in undergraduate education is desirable, and community-oriented approaches have been developed (17, 18), although the potential is largely untapped. Some research projects are likely to be more suitable for undergraduate involvement than others, and identifying those both rich in discovery and accessible to early-career students is challenging (19). The Phage Hunters Integrating Research and Education (PHIRE) program, in which undergraduate and high school students isolate novel bacteriophages, sequence their genomes, annotate them, and analyze them from a comparative genomics perspective, is one response to this challenge (19 – 21). The approach takes advantage of the large, dynamic, old, and highly genetically diverse nature of the bacteriophage population (22, 23). Moreover, although phages play key roles in bacterial pathogenesis (24) and the global climate and ecology (25), we know remarkably little about them outside a few well-studied prototypes. Phages can be easily isolated from the environment, and their relatively small genomes (40 to 150 kbp) are readily sequenced and annotated (26). Phage isolation requires little prior expert knowledge or technical skill, providing an accessible entry point for students from all backgrounds to engage in inquiry-based science (21). Each isolated phage is new, students can name their own phage, and a sense of ownership in their discovery helps to motivate them to explore the secrets of their phage by isolating genomic DNA, determining its sequence, annotating gene predictions, and comparing the sequence to that of other known viruses (21). This programmatic transition from a broadly accessible and concrete introduction to sophisticated genomic analysis provides a rich and structured education platform (27), applicable to STEM and non-STEM students, including first-year undergraduates (28 – 30). To investigate whether the PHIRE approach can be extended to environments beyond the expert phage-focused research laboratory, the Howard Hughes Medical Institute (HHMI), the University of Pittsburgh, and James Madison University investigated a framework enabling broad usage at diverse institutions, involving large numbers of undergraduate students and nonexpert instructors, and assessed its impact. The approach proved to be scalable (4,800 students at 73 schools over 5 years), it was implementable at research-intensive and research-poor institutions, generated gains in phage biology research, and enhanced student retention, and the student-reported gains were equivalent to those from an intense summer research experience. RESULTS The attributes of the PHIRE program at the University of Pittsburgh demonstrate that phage discovery and genomics are a platform that supports engagement of students in authentic research without requiring prior mastery of anything other than very basic concepts and content material (21). We therefore examined whether this could be broadly implemented at institutions with a wide spectrum of missions and demographics, without a requirement for resident expertise in bacteriophage biology. Our core hypothesis was that student participation in this research would generate new insights into phage diversity and evolution while simultaneously elevating student engagement in science, stimulating overall academic performance, and encouraging persistence in STEM fields. Below, we report the structure of the HHMI Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) course and its impacts on both research advances and student learning. The SEA-PHAGES course. The SEA-PHAGES course (formerly called the National Genomics Research Initiative) is a yearlong research experience targeted at beginning college students. Classes typically enroll 18 to 24 students and are taught by one or two faculty members together with a student teaching assistant. In the first term, students isolate phages from locally collected soil samples using Mycobacterium smegmatis as the primary bacterial host, a nonpathogenic strain relevant to understanding Mycobacterium tuberculosis. Students purify and characterize their phages, visualize them with electron microscopy, and extract and purify the DNA. The genome of one phage isolate is sequenced between terms, and in the second term, students annotate the genome using bioinformatics tools to define putative genes, understand genomic arrangements, and predict protein functions. Sequence and annotation quality is expertly reviewed and collated on the PhagesDB database (http://www.phagesdb.org) and submitted to GenBank. The Phamerator program (31) is used to explore genome relationships, and all phage samples are archived for use by the research community. The SEA-PHAGES course curriculum aims to introduce students to research methods and approaches, experimental design, and data interpretation but does not seek to instruct students in content matter outside the immediate biological context. But, as students are direct participants in scientific discovery, the goal is to engage, excite, increase the confidence of, and draw students into a cycle of self-motivation. If successful, we predicted that this would translate into enhanced performance in other STEM classes, greater retention within STEM training, and an increase in the numbers of students seeking continued research experiences beyond their freshman year. Program faculty and teaching assistants are trained at two weeklong workshops, one for each term of the course. Detailed manuals are provided, and community discussions are facilitated by a wiki site. Students and faculty present their findings at an annual SEA-PHAGES Research Symposium, at regional and national meetings, and through peer-reviewed publications. In the 5 years of the program, more than 4,800 students have participated (1,800 in 2012–2013), including STEM majors, non-STEM majors, honors students, and “typical” students. The number of participating schools has grown to more than 70 institutions (see Table S1 in the supplemental material), ranging from community colleges to research universities (Table 1). As can be seen from these program design features, the educational model of the SEA-PHAGES program integrates course-based learning within a framework of scientific activity, including a real-world scientific research agenda, professional networking, and scientific dissemination of results. In this way, the cost-effectiveness of course-based learning is combined with professional science with mutual benefits. TABLE 1  Diversity of institutions participating in SEA-PHAGES Carnegie classification a No. of schools Research universities; very high/high research activity 30 Master’s degree-granting colleges and universities 18 Baccalaureate colleges 22 Associate’s degree-granting colleges 3 a Schools offering the SEA-PHAGES course are organized according to their classification by the Carnegie Foundation for the Advancement of Teaching (2010). Gains in understanding viral diversity. The contributions of the SEA-PHAGES students have been essential to our current understanding of the diversity of mycobacteriophages, demonstrating the substantial impact of the distributed approach compared to what would be accomplished by a single laboratory, and have resulted in several publications with student authors (29, 31 – 39). Since the start of the program in 2008, SEA-PHAGES students have isolated 3,000 new phages (with global positioning system [GPS] coordinates recorded) and characterized their phages by DNA restriction analysis and electron microscopy. More than 450 mycobacteriophage genomes have been sequenced and annotated, and more than 350 sequences have been deposited in GenBank (Fig. 1). These genomes include many distinctly different types and numerous complex variants (40), and the entire genome collection codes for over 48,000 genes representing 3,780 sequence phamilies (a group of proteins sharing similarity to at least one other above threshold BlastP and Clustal values [31]). Correlations between genome and geography or time of isolation have been explored (35, 41), as well as the evolutionary mechanisms contributing to the pervasive genome mosaicism (33). The genomes contain numerous examples of biological intrigue, including novel inteins, introns, mobile elements, immunity systems, and regulatory schemes (33 – 35, 42 – 45), as well as potential for developing new tools for understanding tuberculosis (46 – 49). FIG 1  SEA-PHAGES students contribute to scientific knowledge. Results are from the first 5 years of the SEA-PHAGES program isolating new phages, showing the cumulative numbers of phages isolated (blue), cumulative numbers of genomes sequenced (orange), cumulative numbers of gene phamilies (purple), and total numbers of mycobacteriophages in GenBank (green). Not all genomes sequenced and annotated in year 5 are yet available in GenBank. The diversity of phages known to infect a single common host is remarkable; there are many thousands of potential bacterial hosts for phage isolation, and host range studies suggest that simply using a different strain of the same bacterial species will result in distinct profiles of diversity (38). With an estimated 1031 phage particles in the biosphere and a population that turns over every few days (23), there is an inexhaustible reservoir for discovery. Impacts on student education and retention. The Survey of Undergraduate Research Experience (SURE) and the Classroom Undergraduate Research Experience (CURE) measure the students’ assessment of their understanding of science and scientists, confidence in their ability to perform research, and their perceived gains in skills (50). The self-perceptions of learning gains, motivation and attitude, and career aspirations of the SEA-PHAGES course participants were assessed with pre- and postcourse SURE-like surveys (see Fig. S1 in the supplemental material). Twenty of the SEA-PHAGES survey items are shared with the regular SURE and CURE surveys, allowing the comparison of the SEA-PHAGES students’ learning gains with those of students who engaged in a dedicated summer research experience (SURE) and students who completed traditional science courses with no research element (CURE) (Fig. 2). The SEA-PHAGES students scored as well as or better on all 20 learning gains compared to the SURE students, reflecting benefits at least equivalent to those accrued through a summer-long apprentice-based undergraduate research experience. The increase in scientific self-efficacy reported by the SEA-PHAGES students is likely to be directly related to their retention in science (51). FIG 2  Student evaluation of learning gains. Mean learning gains for common survey items on the SURE (green diamonds), CURE (blue squares), and the SEA-PHAGES (red triangles) assessment instruments are shown. The SURE survey data represent 2,358 students who completed summer research in 2009; the CURE survey data represent 476 students who were enrolled in science courses that were described by their instructors as without a research element (data collected for fall 2007 through spring 2009); the SEA-PHAGES data represent 121 students who evaluated their course following the academic year 2008–2009. Error bars represent 2 standard errors around the mean. To analyze the effect of the SEA-PHAGES course on student persistence, we compared retention of students enrolled in the SEA-PHAGES course (77% first-year students and 95% STEM majors) with two benchmark statistics: the retention of all students and the retention of STEM majors with the same number of years of college experience and enrolled at the same school (Fig. 3A), important parameters given the typical rates for student attrition between first- and second-year STEM undergraduates (52). Data were from 27 comparisons from 20 institutions and show clearly that SEA-PHAGES students matriculated into the second year at significantly higher rates than did either benchmark group. Thus, early engagement in a research experience improves student retention into the second year. The positive impacts of this course-based research experience are similar to what has been reported for apprentice-based research experiences (5, 53), represent an effective response to the call to action in the National Science Foundation (NSF) Vision and Change and PCAST reports (1, 4), and provide validation for this educational model on a larger scale. FIG 3  (A) Retention of SEA-PHAGES participants (red) compared to other students at the same institution (blue), year 1 to year 2 of their college experience. Retention data were gathered from 20 institutions, with some institutions contributing data from multiple years, resulting in 27 sets of comparison data. Retention data were analyzed with a between-group analysis of variance with 3 levels of the independent variable (all majors, STEM majors, and SEA-PHAGES students) for 171 reports. The result was interpreted as significant at the 0.05 level. (B) SEA-PHAGES students (red) perform better than peers (blue) in traditional laboratory sections in the introductory lecture course. Results are for 127 SEA-PHAGES students and 1,120 students in the traditional laboratory course from six institutions. In the lecture course, SEA-PHAGES students averaged 2.95 on a 4.0 scale, compared to the 2.58 average of students in traditional lab sections. This difference was significant (t = 2.64; P < 0.05). Anticipating that research-stimulated motivation will influence student performance in other courses, we selected six schools that substituted the SEA-PHAGES course for a regular biology laboratory and compared the grades of participating students in the accompanying biology lecture course (Fig. 3B). We limited this analysis to schools that enrolled “typical” students into the PHAGES lab sections rather than those aimed at honors students or students at academic risk. The biology lecture course grades of SEA-PHAGES students were compared directly to those of peers enrolled in the same lecture course but in the regular biology laboratory. As is the case with most applied research, students were not randomly assigned to conditions, and even among these “typical” students, there may have been some self-selection for registration in the SEA-PHAGES course. We observed substantial differences in both the average grades and the grade distribution of SEA-PHAGES students relative to those of students in traditional lab sections (Fig. 3B), and although these data are preliminary and warrant further study, they suggest that there could be broad educational benefits to the SEA-PHAGES experience. Because of the concern that SEA-PHAGES students might suffer from lack of exposure to a broader coverage of subject matter in the regular laboratory course, we developed a 25-item pre- and postcourse survey of biological concepts (see Fig. S2 in the supplemental material) which was administered to students before and after the laboratory courses. There was no significant difference in performances on the test between SEA-PHAGES students and the comparison group of students (see Fig. S3). Both groups improved from pretest to posttest, and there was no significant difference between the groups in terms of the extent of their improvement. The lack of exposure to additional topics in the SEA-PHAGES course thus had no obvious detrimental effect. DISCUSSION The HHMI SEA-PHAGES program provides a general model for accomplishing improvements in the persistence of students in science by transforming a small-scale scientific inquiry into a cross-institution education platform that engages first-year students. The outcomes are consistent and robust, benefitting diverse groups of students across a variety of institutions. The materials costs are similar to those of other inquiry-based courses, and many institutions have implemented the course without external support, other than assistance with sequencing costs and programmatic and scientific support from HHMI and the University of Pittsburgh (some schools received direct external support for materials during their first 3 years in the program). The size and diversity of the phage population provide an inexhaustible wealth of biological novelty that imposes no obvious limit on the number of students who can participate. Future opportunities include further broadening the implementation of the SEA-PHAGES course as well as extending the model to development of similar projects in which scientific discovery, project ownership, and simple entry points can be implemented at the first-year college level. Meeting these opportunities will lead to a broad and sustainable enhancement of undergraduate science education, an advancement of scientific knowledge, and an increase of student persistence in science. MATERIALS AND METHODS Participants. The study was conducted with SEA-PHAGES faculty and students in the United States and the Commonwealth of Puerto Rico. David Lopatto and participant institutions obtained appropriate institutional review board (IRB) approval. SEA-PHAGES faculty are trained in a weeklong workshop focusing on in situ procedures and pedagogy in preparation for the fall semester and a weeklong workshop focusing on in silico bioinformatics tools in preparation for the spring semester. Faculty and students are invited to a SEA-PHAGES National Symposium to present their scientific findings. The SEA office conducts annual site visits and provides continuous technical support for institutions year-round. The SEA Wiki maintains an up-to-date depository for announcements, communication forums for faculty and students, curriculum resources, instructional materials, and research archives. SEA-PHAGES faculty members recruited comparison group students on a volunteer basis to enhance the validity of statistical analysis. The comparison group students were recruited among students taking introductory laboratory courses. Except for the student grade analysis, comparison group students cannot be matched to SEA-PHAGES students on each campus, so statistical analysis was limited to quasiexperimental analysis based on a nonequivalent comparison group. Systemic Research sent out invitations to all consenting students’ e-mail addresses individually. Analysis. During academic year 2009–2010, different aspects of the SEA-PHAGES and comparison group were measured. White/Caucasian students made up the majority of each group, 66% of SEA-PHAGES students and 76% of comparison group students. The majority of both groups lived in suburban communities (66% SEA-PHAGES and 64% comparison group students), attended public high schools (83% SEA-PHAGES and 83% comparison group students), and were in their first year in college (SEA-PHAGES, 77% first-year students, 18% sophomores; comparison group, 70% first-year students, 20% sophomores). There were a higher percentage of male students in the SEA-PHAGES course (38%) than in the comparison group (29%), but in both groups, female students were the clear majority. Retention rates. The Institutional Annual Survey measures student retention rates by tracking full-time, first-time entering students who are seeking bachelor’s degrees. The Institutional Annual Survey was conducted among institutions during November to December. Retention rates were calculated for students returning in fall 2008 and fall 2009. An analysis of variance was performed over 3 groups (all majors, STEM majors, and SEA-PHAGES students). The data were reported by institution and category, including 63 reports for all majors, 43 reports for STEM majors, and 65 reports for SEA-PHAGES students. The SEA CURE survey. The Classroom Undergraduate Research Experience (CURE) survey was specially adapted to the SEA-PHAGES program by David Lopatto (Grinnell College, Grinnell, IA). The CURE survey consists of multiple sections, including institution, class, demographics, science-related activities, major and minor concentration, postgraduate academic goals, experiences in laboratory course elements, experience in research, engagement in activities or endeavors, course benefit, learning experience in laboratory experiments and tools, overall course evaluation, and opinions about science. Systemic Research added a few questions to the postcourse CURE survey to collect data regarding students’ SEA-PHAGES course satisfaction, SEA Wiki access and utilization, SEA-PHAGES research paper and presentation experience, and general comments. The survey was administered twice a year: the presurvey at the beginning of the fall semester and the postsurvey at the end of the spring semester. As with the Biological Concepts Survey (BCS), Systemic Research developed the online survey forms using the Vovici EFM Community Professional website. The pre- and postcourse survey invitations were e-mailed to individual students according to their academic calendars. Using Vovici’s survey follow-up feature, three reminder e-mails were sent after the initial invitations. The collected survey responses were securely saved in a dedicated Vovici HHMI website and Systemic Research’s NGRI student database. The SURE survey data represent 2,358 students who completed summer research in 2009; the CURE survey data represent 476 students who evaluated science courses that were described by their instructors as without a research element (data collected fall 2007 through spring 2009); the SEA-PHAGES data represent 121 students who evaluated their course following the academic year 2008–2009. Mean learning gains were calculated for each category of the 20 items common to both the CURE and SURE surveys. Grades. Eleven institutions submitted their SEA-PHAGES students’ laboratory and introductory biology course performance data for fall 2008 and spring 2009 in the academic year 2008–2009 and fall 2009 and spring 2010 in the academic year 2009–2010. Letter grade distributions for both SEA-PHAGES and comparison students were collected. Six institutions had matched data that were utilized in the analysis, with 127 SEA-PHAGES and 1,120 comparison student grades. For statistical analysis, the letter grades were assigned numerical values from 4 (grade A) to 0 (grade F). t tests were performed comparing the mean grades received by SEA-PHAGES students and comparison group students in the biology lecture course. Biological methods. Mycobacteriophage isolation was performed using Mycobacterium smegmatis mc2155 as a host, and phages were identified as PFU either by direct plating on bacterial lawns or after enrichment in the presence of M. smegmatis. Following purification and amplification, DNA was isolated and sequenced using Sanger, 454, or Ion Torrent technologies, using a shotgun approach followed by targeted sequencing to validate ambiguities and determine genome ends. Genome annotations were performed using various software platforms, including GBrowse (54), Apollo (55), DNAMaster (http://cobamide2.bio.pitt.edu/), Glimmer (56), GeneMark (57), and analysis programs available at the National Center for Biotechnology Information (NCBI). Comparative genomics used Phamerator (31) and Gepard (58). Assembled genome sequences and genome annotations were subjected to expert review prior to submission to GenBank. Detailed methods for phage isolation, sequencing, and analysis are available on PhagesDB (http://phagesdb.org). SUPPLEMENTAL MATERIAL Figure S1 SEA-CURE postsurvey. Download Figure S1, PDF file, 0.2 MB Figure S2 Biological Concepts Survey (BCS) questions. Download Figure S2, PDF file, 0.3 MB Figure S3 Biological Concepts Survey results. Download Figure S3, PDF file, 0.1 MB Table S1 Institutions offering the SEA-PHAGES course from 2008 to 2013. Table S1, PDF file, 0.1 MB.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Improving Underrepresented Minority Student Persistence in STEM

              Members of the Joint Working Group on Improving Underrepresented Minorities (URMs) Persistence in Science, Technology, Engineering and Mathematics (STEM), utilizing Kurt Lewin’s planned approach to change, describe five recommendations to increase URM persistence in STEM at the undergraduate level.
                Bookmark

                Author and article information

                Contributors
                Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: Writing – review & editing
                Role: Formal analysisRole: Writing – review & editing
                Role: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: Formal analysisRole: Funding acquisitionRole: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Role: Formal analysisRole: Funding acquisitionRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 November 2019
                2019
                : 14
                : 11
                : e0224288
                Affiliations
                [1 ] Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, United States of America
                [2 ] Microbiology and Cell Science Department, University of Florida, Gainesville, FL, United States of America
                [3 ] Department of Agricultural Education and Communication, University of Florida, Gainesville, FL, United States of America
                [4 ] Department of Biology, Agnes Scott College, Decatur, GA, United States of America
                [5 ] Department of Biology, San Diego State University, San Diego, CA, United States of America
                [6 ] Department of Biology, College of Wooster, Wooster, OH, United States of America
                [7 ] University of California, Riverside, Riverside, CA, United States of America
                [8 ] Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, United States of America
                [9 ] Department of Biological Sciences, Hampton University, Hampton, VA, United States of America
                [10 ] Department of Chemistry and Biochemistry, California Polytechnic State University, San Luis Obispo, CA, United States of America
                [11 ] Department of Teacher Education, University of Nebraska at Omaha, Omaha, NE, United States of America
                [12 ] Department of Biological Sciences, North Carolina State University, Raleigh, NC, United States of America
                [13 ] Department of Biological Sciences, Bioinformatics Program, St. Edward’s University, Austin, TX, United States of America
                [14 ] Departments of Biological Sciences and Mathematical Sciences, University of Delaware, Newark, DE, United States of America
                [15 ] Department of Biology, Lycoming College, Williamsport, PA, United States of America
                [16 ] Department of Biochemistry and Molecular Genetics, University of Virginia School of Medicine, Charlottesville, VA, United States of America
                [17 ] Biology and Biotechnology Department, Worcester Polytechnic Institute, Worcester, MA, United States of America
                [18 ] Bioinformatics Program, Saint Vincent College, Latrobe, PA, United States of America
                [19 ] Digital World Biology, PMB, Seattle, WA, United States of America
                [20 ] Department of Natural Sciences, Inter American University of Puerto Rico, Metropolitan Campus, San Juan, PR, United States of America
                [21 ] Department of Biology, University of Nebraska at Omaha, Omaha, NE, United States of America
                [22 ] Department of Biology, Susquehanna University, Selinsgrove, PA, United States of America
                [23 ] Department of Biology, Chemistry, and Environmental Sciences, Inter American University of Puerto Rico, San Germán Campus, San Germán, PR, United States of America
                [24 ] Department of Computer Science, Ohio University, Athens, OH, United States of America
                [25 ] School of Life Sciences, Arizona State University, Tempe, AZ, United States of America
                [26 ] Center for New Designs in Learning and Scholarship, Georgetown University, Washington, DC, United States of America
                [27 ] Department of Biology, Georgetown University, Washington, DC, United States of America
                [28 ] School of Interdisciplinary Informatics, University of Nebraska at Omaha, Omaha, NE, United States of America
                Universidade de Mogi das Cruzes, BRAZIL
                Author notes

                Competing Interests: We declare that author TMS has an affiliation with a private company, Digital World Biology (DWB). As noted in the Funding Statement, DWB provided support for this work in the form of salary for TMS. This affiliation does not alter our adherence to PLoS ONE policies on sharing data and materials.

                [¤a]

                Current address: National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, San Juan, PR, United States of America.

                [¤b]

                Current address: Division of Undergraduate Education, Directorate for Education and Human Resources, National Science Foundation, Alexandria, VA, United States of America.

                ‡ These authors also contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-0296-6015
                http://orcid.org/0000-0003-0495-4840
                http://orcid.org/0000-0002-6493-940X
                http://orcid.org/0000-0002-2614-0285
                http://orcid.org/0000-0003-1308-0321
                Article
                PONE-D-19-17542
                10.1371/journal.pone.0224288
                6860448
                31738797
                24fcbae0-425c-4feb-80ff-f132eaa35497

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 20 June 2019
                : 9 October 2019
                Page count
                Figures: 9, Tables: 5, Pages: 19
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1539900
                Award Recipient :
                This material is based upon work supported by the National Science Foundation under Grant no. 1539900 to E.D., M.W., A.G.R., E.W.T., and W.T. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. A commercial company, Digital World Biology, provided support in the form of salary for author TMS but did not have any additional role in the study design, data collection, and analysis, decision to publish, or preparation of the manuscript. The specific roles of this author are articulated in the "author contributions" section.
                Categories
                Research Article
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                People and Places
                Population Groupings
                Educational Status
                Undergraduates
                Biology and Life Sciences
                Research and Analysis Methods
                Research Design
                Survey Research
                Surveys
                Social Sciences
                Sociology
                Education
                Schools
                Colleges
                Computer and Information Sciences
                People and Places
                Population Groupings
                Educational Status
                Graduates
                Social Sciences
                Sociology
                Education
                Workshops
                Custom metadata
                Data are available on the NIBLSE respository on GitHub, https://github.com/niblse.

                Uncategorized
                Uncategorized

                Comments

                Comment on this article