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/
), 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
) 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
), 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
). 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.
MATERIALS AND METHODS
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.
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.
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.
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.
Mycobacteriophage isolation was performed using Mycobacterium smegmatis
155 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