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Advancing Equity and Inclusion in Microbiome Research and
Training
Alicia J. Foxx,
a
Karla P. Franco Meléndez,
a
Janani Hariharan,
b
Ariangela J. Kozik,
c
Cassandra J. Wattenburger,
b
Filipa Godoy-Vitorino,
d
Adam R. Rivers
a
a
U.S. Department of Agriculture, Agricultural Research Service, Gainesville, Florida, USA
b
Cornell University, Ithaca, New York, USA
c
University of Michigan, Ann Arbor, Michigan, USA
d
University of Puerto Rico, School of Medicine, San Juan, Puerto Rico, USA
Karla P. Franco Meléndez, Janani Hariharan, Ariangela J. Kozik and Cassandra J. Wattenburger contributed equally to this work.
ABSTRACT This article proposes ways to improve inclusion and training in microbiome
science and advocates for resource expansion to improve scientific capacity across insti-
tutions and countries. Specifically, we urge mentors, collaborators, and decision-makers
to commit to inclusive and accessible research and training that improves the quality of
microbiome science and begins to rectify long-standing inequities imposed by wealth
disparities and racism that stall scientificprogress.
KEYWORDS collaboration, equity, inclusion, international, mentoring, microbiome,
training
MAKING THE CASE FOR EQUITY IN MICROBIOME SCIENCE
Microbiome research is being applied to important global challenges like pan-
demic preparedness, infectious disease prevention, climate change, and food se-
curity. This research is currently concentrated in a few resource-rich countries (1) which
limits the field in several ways. The best solutions to these global challenges come
from the work of scientists who understand the cultural and logistical needs of imple-
menting solutions in their communities. The microbiomes of natural, host-associated,
and built environments vary geographically, so undersampling large regions of the world
limits our understanding of microbial communities (2, 3). This leaves a valuable subset of
the microbial biosphere uncharacterized and a valuable subset of researchers excluded.
Changes to microbiome science that increase scientific opportunities for persons histori-
cally excluded due to ethnicity and people from low- and middle-income countries will
improve the quality of research in the field as well as being the right thing to do.
UNIQUE AND SHARED CHALLENGES FOR PEER AND LMIC MICROBIOME
SCIENTISTS
Persons who identify as Black or African American, Latinx or Hispanic, and peoples
indigenous to land comprising the United States and its territories (henceforth called
PEERs for persons excluded due to ethnicity or race) (4, 5) have been excluded from,
and therefore underrepresented in microbial science, and the sciences more broadly.
Scientists from low- and middle-income countries (LMICs) are similarly underrepre-
sented in contemporary science. To make microbiome science global, equitable, and
inclusive, and thus serve everyone, we explicitly focus on support for PEER and LMIC
scientists and trainees. These groups differ in the challenges they face for different
socio-political reasons, but we identify common needs and advocate for changes and
resources aimed at improving inclusion and access to microbiome research. This article
Citation Foxx AJ, Franco Melendez KP,
Hariharan J, Kozik AJ, Wattenburger CJ, Godoy-
Vitorino F, Rivers AR. 2021. Advancing equity
and inclusion in microbiome research and
training. mSystems 6:e01151-21. https://doi
.org/10.1128/mSystems01151-21.
Editor Benjamin E. Wolfe, Tufts University
This is a work of the U.S. Government and is
not subject to copyright protection in the
United States. Foreign copyrights may apply.
Address correspondence to Alicia J. Foxx,
alicia.foxx@usda.gov, or Adam R. Rivers,
adam.rivers@usda.gov.
This piece proposes ways to improve
inclusion and training in microbiome science
and urges decision-makers to commit to
rectifying long-standing inequities imposed by
wealth disparities and racism that stall scientific
progress
Published 12 October 2021
September/October 2021 Volume 6 Issue 5 e01151-21 msystems.asm.org 1
PERSPECTIVE
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is intended to start a conversation within the microbiome community, and we provide
resources for persons in decision-making positions (e.g., principal investigators, men-
tors, collaborators, funders, administrators, professional societies) to implement and
invest in equity in science and health (Fig. 1).
PEER scientists. The systematic exclusion of PEERs from academic and scientific
pursuits contributes to the persistent underrepresentation of PEER individuals in the
microbial sciences (4, 6). Decades of efforts have failed to lead to major, sustained
increases in representation of PEER scientists, especially in leadership roles and other
positions of influence; this is especially acute in microbiology (7). Recent critiques have
highlighted the need to shift narratives (and therefore solutions) away from a deficit
framework and toward making changes to institutions themselves. A deficit framework
focuses only on diversity and emphasizes a perceived lack of ability or “fit”of PEER indi-
viduals. However, improvements can be made by prioritizing the transformation of teach-
ing, training, and research environments to better serve PEER individuals and an organiza-
tion as a whole (8). This transformation requires a commitment to equity and inclusion
that includes stakeholders at all levels and a willingness to identify and address structural
and systemic barriers (9). Challenges exist at every step from recruitment into undergradu-
ate and graduate training through promotion and tenure (10–12), mentoring (13, 14),
FIG 1 Decision-makers, key areas of change within the microbiome sciences, and actions that will foster
inclusion for PEER and LMIC scientists in microbiome sciences.
Perspective
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appointment to leadership positions (7, 15), career development for nonacademic pursuits
(16, 17), publishing (18–21), and acquisition of funding (22–25). However, PEERs in the mi-
crobial sciences are expected to persist despite cultures that devalue them and their tal-
ents. The institutions that have historically served PEER scientists like American community
colleges, tribal colleges, and historically black colleges and universities often contend with
reduced access to resources and infrastructure needed to train students in computing and
communication skills (26–28). There is a need for bold, resourced, and strategic programs
that support the careers and training of PEERs in microbiome sciences, their matriculation
to leadership positions, and the transformation of programs, departments, and organiza-
tionstoensureinclusivecultureswhereeveryonecanthrive.
LMIC scientists. Like PEER scientists, LMIC scientists bring a wealth of talent, ideas,
and perspectives that would enrich the scientific process and culture, and yet, researchers
from both groups often lack opportunities to acquire the training, funds, and support to
make significant contributions to their fields. Countries holding economic and technologi-
cal wealth must cooperate synergistically with LMICs to promote their participation and
leadership in research for a more globally inclusive microbiome training agenda (29–32).
In Table 1, the “Guidelines for equitable collaboration and mentoring practices with LMIC
and PEER scientists”detail resources that have been successfully used toward developing
guidelines that promote equitable research collaborations between well-funded research
TABLE 1 Organizational resources and examples of equitable research and mentoring practices with LMIC and PEER scientists and trainees
Theme Resources
Guidelines for equitable collaboration and
mentoring practices with LMIC and PEER scientists
Montreal Statement on Research Integrity in Cross-Boundary Research Collaborations (33):
guidance on agreements and responsibilities when engaging in cross-national, -institutional,
and -disciplinary research
The Swiss Commission for Research Partnership with Developing Countries (34) and The
Research Fairness Initiative (35, 36): organization and program for equitable collaboration
with LMIC scientists
The Nagoya Protocol (37): equitable access and benefit-sharing of genetic resources
National Academy of Sciences, Engineering, and Medicine mentoring report (38): guidance on
inclusive mentoring practices
IDEA Network of Biomedical Research Excellence (INBRE): support for research, mentoring,
collaboration. and faculty training in Puerto Rico (http://inbre.hpcf.upr.edu/bioinformatics
-resource-core/)
Microbiome-focused equitable partnerships The Earth Microbiome Project (39): a global initiative focused on the development of standard
operating procedures for the characterization of the earth microbiome
The international Human Microbiome Standards (https://cordis.europa.eu/project/id/261376): a
global initiative focused on the development of standard operating procedures for the
characterization of the human microbiome
The Benioff Center for Microbiome Medicine (https://microbiome.ucsf.edu/commitment
-diversity-equity-and-inclusion): example of PEER support and in microbiome sciences
Team building and communication resources Cold Spring Harbor Laboratory Leadership in Bioscience Workshop (https://meetings.cshl.edu/
courses.aspx?course=c-leader&year=19): workshop on effective leadership and mentoring in
science
EMBO Laboratory Leadership course (https://lab-management.embo.org/): leadership courses
with an emphasis on research and research dissemination
Springer Nature Effective Collaboration course (https://masterclasses.nature.com/online-course
-effective-collaboration-in-research/17078834): course on effective collaboration in science
UCSF The Scientific Leadership and Management Skills course (https://postdocs.ucsf.edu/slms):
example of a leadership program for postdoctoral researchers in sciences
Microbiome training and conference-based support
for LMIC and PEER scientists
International Society for Microbial Ecology (https://www.isme-microbes.org/ambassadors):
Ambassador program with global organizations for workshops and activities
The Microbiota Vault (https://www.microbiotavault.org) and MV-Global Microbiome Network
(GloMiNe) symposia: example of global symposium with the goal of education to promote
preservation of microbial ecosystems in nature and in collections
Codes of ethics at conferences to support underrepresented scientists (40)
Guidelines for organizing an intentional bioinformatics training in LMIC (41)
Perspective
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institutions and LMIC scientists. When establishing global partnerships for microbiome
research, consider following the guidelines and successful examples detailed in Table 1.
Existing international programs in microbiome surveying (Table 1, “Microbiome-focused
equitable partnerships”) show that equitable partnerships in this field are not only possible
but are successful through sharing of resources, project responsibilities, and funding. Their
contributions to the field include significant microbiome curation efforts, including the
design of standard protocols for sample collection and processing, data analysis, and data
sharing (39). We propose that these and other international working groups, already at the
forefront of microbiome research, serve as exemplars in the creation of guidelines for in-
clusive and equitable collaborations with LMIC scientists.
We also highlight more specific pathways toward training and research practices
that enrich the experiences of both LMIC and PEER scientists that scientists from high-
income countries (HIC) can take up. For mentoring and collaboration, HIC scientists
can create mentoring communities with more than one mentor to provide various per-
spectives for PEER and LMIC mentees (38) and understand and dismantle power dy-
namics associated with privilege within PEER mentorship. Mentors and collaborators
from positions of privilege should counteract factors that negatively affect mentees’expe-
riences (e.g., combating institutional racism) and should employ culturally responsive men-
toring and collaboration which embraces questions asked by PEER and LMIC scientists
that are important to their cultural identities but may differ from norms set by Western or
white scientists (38, 42–46). These scientists should engage in mentor and collaborator
training such as team-building courses to communicate roles and responsibilities effectively
and improve team productivity (Table 1, “Team building and communication resources”)
and should model expectations for an inclusive environment and practice transparent and
impartial conflict resolution (38, 42–46). However, all team members, regardless of identity,
should understand their own cultural identities and biases and how they impact the team.
Towards equitable research practices, scientists from HIC should actively apply for
international grant funding opportunities which foster microbiome studies with LMIC
scientists (e.g., the NIH Fogarty International Center) and while doing so, should dis-
cuss ownership of data and authorship of publications with trainees and collaborators,
support the active participation of LMIC scientists in designing microbiome studies
and avoid “helicopter research”in which HIC scientists travel to conduct research in an
LMIC with little or no involvement of local scientists. This is a practice that has become
worryingly common as global collaborations increase (47). Collaborating with, rather
than extracting from, communities or regions under study helps to decolonize science
(48). This means including LMIC and PEER scientists as coauthors and not just mention-
ing them in the acknowledgments and avoiding exploitation of their knowledge and
labor, identifying research needs for these communities, or taking local specimens
with limited engagement.
ADDRESSING LANGUAGE AND COMMUNICATION BARRIERS
Scientists from different fields, cultures, and languages must be able to clearly com-
municate with each other to discover connections between ideas and develop sustain-
able collaborations to advance the microbiome sciences. We urge support for virtual
training programs that include efforts to create resources in multiple languages like
translation of programming tutorials of The Carpentries training organization into
Spanish. Current technology translates virtual resources and provides closed caption-
ing in real time which accommodates scientists with disabilities and nonnative speak-
ers. We also urge funding agencies and professional societies to allocate resources for
translating conference materials and to host multilingual workshops, particularly to
highlight research performed by LMIC scientists (Table 1, “Microbiome training and
conference-based support for LMIC and PEER scientists”). Virtual conferences have
increased access for scientists who cannot easily travel due to accessibility issues, fam-
ily commitments (49), visa requirements, and funding limitations that disproportion-
ately limit LMIC scientist’s participation in training, symposia, and conferences. One
Perspective
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notable success has been the National Summer Undergraduate Research Program
(NSURP), a paid virtual research program that has successfully recruited microbiologists to
mentor PEER students from the United States, providing a completely online microbial
training experience and professional development opportunities (10). Since this program
currently reaches a limited number of mentees, we call for funding to expand such initia-
tives and their scope to serve trainees across geographical boundaries; increased funding
would increase the program’s reach as well as allowing for international trainees to partici-
pate. For all trainees, including PEER microbiome scientists, science outreach at community
venues like schools, science centers, and museums, helps build communication skills.
Science outreach also positively impacts the communities by enhancing interest and
engagement in science and offering role models representative of students’social identi-
ties (50, 51), which can lead to higher recruitment of PEER scientists in STEM (science, tech-
nology, education, and mathematics) (52). We also recommend that academic programs
incentivize students with credits, certification, or awards to participate in outreach events
and science communication classes as part of their training (for examples, see Table S1 in
the supplemental material).
INCREASING ACCESS TO MICROBIOME TECHNOLOGY AND PUBLISHING
Microbiome data sets are large, and their analysis requires expertise in molecular
biology, microbiology, and computational biology. The extraction of nucleic acids from
samples can be done with standard molecular biology equipment, but the generation
and interpretation of these data typically require access to expensive reagents,
sequencing services, and computer clusters which is often a barrier for scientists from
LMICs. We present resources that could reduce financial and technological barriers to
sequencing and provide free resources to high-performance computing for micro-
biome research in Table S1. These resources are primarily published modifications to
standard protocols for sample preservation, DNA extraction, library preparation, and
multiplexing that reduce costs at each step in the process. Sequencing itself remains a
financial barrier, but a few programs like the U.S. Department of Energy Joint Genome
Institute’s Community Science Program provides access to sequencing and advanced
microbiome methods to scientists anywhere in the world through a grant-based, user
facility model. Free, cluster-based metagenomics computing resources are available
through Kbase, Xcede, Cyverse, MGnify, and MG-Rast (53–56). In the longer term, work
should be publicly funded to develop and nonexclusively license a suite of low-cost,
validated, open-source protocols for preservation, extraction, and library preparation.
This could radically lower costs of sample preparation and thereby increase access and
equity, create new products, and open new lines of microbiome research, especially if
supported by public sector investment and technology transfer.
Microbiome data sets are large and multivariate, and analyzing these data effec-
tively requires specialized training. Data analysis training should be made accessible to
LMICs so that in silico experiments are supported alongside training of bioinformati-
cians who are comfortable using and developing projects with sequence data. We also
recommend the creation of online “code clubs”(57) or cross-institutional working
groups who learn to code and analyze data together. Such clubs enable peer learning,
foster opportunities for research collaborations, and provide resource and skill-sharing
between institutions with unequal economic access.
In addition to lack of access to technology, the high cost of publication in science
can be a barrier to LMIC scientists in particular (58). Some microbiome research jour-
nals offer free publication, or fee waivers or cost reductions for scientists from LMICs
(for a list of journals, see Table S2). Publishing in high-impact open-access journals con-
stitutes approximately 6 months’salary of African scientists, and government and uni-
versities do not cover these fees (59). While fee waivers exist, the processes are veiled
and need transparency, and other journals, including society journals, must consider
providing free publishing mechanisms. Sharing research as preprints is now standard
practice in fields like physics, and microbiome research would benefit from a similar
Perspective
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adoption. Preprints offer the opportunity to make research rapid and more transpar-
ent, though they may require careful evaluation prior to being peer reviewed.
Open science will allow PEER and LMIC trainees to learn key data analysis skills, con-
tribute new research, and further their careers through the meta-analysis of previously
published microbiome data in the absence of funding to produce new data. However,
this requires both freely available data sets and high-quality metadata. Some federal
agencies are addressing issues associated with data accessibility by recommending
data sharing upon request (60). Transparency can also be reinforced by making sure that
accepted manuscripts provide accessible, high-quality, accessioned raw data and provide
metadata spreadsheets compatible with microbiome data management software (e.g., for
Qiita and European Bioinformatics Institute [EBI]). Funding agencies, journals, and reposito-
ries should require and provide incentives to enforce high-quality submission standards,
allow data sets to be cited, and provide better tutorials and consistent submission expecta-
tions across databases to normalize open-science practices for microbiome data (61).
CALL TO ACTION
Shifting the research culture in microbiome science by making research and train-
ing more inclusive will improve retention of underserved scientists and contribute to
the field’s intellectual growth. Such endeavors are opportunities to broaden our per-
spectives of how the environment, social identity, biopsychosocial factors, and cultural
practices affect microbiome science around the world but are also imperative to
restore equity and social justice in the field. We urge collaborators, mentors, funders,
and decision-makers in resource-rich countries to take concrete actions to improve the
inclusiveness of microbiome science (Fig. 1). Changing cultural norms can take time,
but implementing even small improvements can create a considerable difference for a
trainee or collaborator. As microbiome scientists, we call on other members of the
community to set an example of inclusivity and accessibility for the broader scientific
community.
SUPPLEMENTAL MATERIAL
Supplemental material is available online only.
TEXT S1, DOCX file, 0.02 MB.
TABLE S1, DOCX file, 0.01 MB.
TABLE S2, DOCX file, 0.02 MB.
TABLE S3, DOCX file, 0.02 MB.
ACKNOWLEDGMENTS
We thank Ana Maldonado-Contreras, Monika Oli, and Maria Gloria Domínguez-Bello
for discussion and ideas for this article. We thank Ben Wolfe, Emily Delorean, and Ashley
Schoon for feedback for reviewing drafts of this paper.
A.J.K. is supported in part by KL2TR002241 and UL1TR002240. A.J.F. is supported in
part by an appointment to the Agricultural Research Service (ARS) Research Participation
Program administered by the Oak Ridge Institute for Science and Education (ORISE)
through an interagency agreement between the U.S. Department of Energy (DOE) and
the U.S. Department of Agriculture (USDA). ORISE is managed by ORAU under DOE
contract number DE-SC0014664.
The findings and conclusions in this publication are those of the authors and should
not be construed to represent any official determination or policy of the USDA, U.S.
Government, or any of the entities which contributed funding.
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