An Ocean Microbiome Initiative at WHOI The Ocean Microbiome. A microbiome is a group of primarily unicellular organisms that operates as a
consortium to effect specific organismal, geochemical, or ecosystem processes. In a microbiome,
microbes occupy niches that compete with, or complement, those of their neighbors. Their organism-level
exchange of chemicals and substrates generates widely observed patterns reflecting and governing global
biogeochemical cycles. Marine microbiomes include surface- and deep-ocean microbial loops, particleassociated consortia, symbionts of faunal hosts, or sediment- and bedrock-hosted communities. Together,
these communities mediate a vast array of chemical and biological reactions, culminating in the elemental
cycles and fluxes that control the function and health of the oceans.
Microbiome research in the oceans has strong parallels with microbiome research in all other
environments. In general, microbiome research is centered on exploration of the physiology of, and
interactions among, microbes within complex consortia. Whether focused on the human gut or the marine
biological pump, investigations seek to understand the roles of microbial diversity (who is there?), their
physiologies (what are they doing?), and their metabolites (what are they making?) in directly or
indirectly controlling the health and function of the host or surrounding biogeochemical environment.
Further, studies seek to define interactions among consortia members, their impact on net community
function and their resilience and response to external perturbations. Microbiome research is inherently
interdisciplinary, combining ecology, physiology, microbiology, chemistry and modeling to understand
these critical biomes.
National Microbiome Research. Recently, attention has focused on microbiome research as a new
integrative approach to studying human health, energy generation and preservation of the environment.
Papers in Science and Nature have proposed an integrative research program in the microbiomes of
disparate environments, including the oceans. With the BRAIN initiative as an example, funding agencies
and private foundations appear to be mobilizing resources in anticipation of a national Unified
Microbiome Initiative. WHOI scientists have a golden opportunity, therefore, to coalesce around themes
that could serve as the foundation for a future WHOI initiative, as well as integrative grant applications to
new funding sources.
WHOI’s Competitive Edge. Investigators at WHOI have long been involved in microbiome research,
seeking to integrate microbial perspectives with marine biogeochemical cycles. Biologists Holger
Jannasch, Stanley Watson, and John Waterbury pioneered the observation and cultivation of marine
microbes from diverse environments. Over the years, a rich tradition has developed in biogeochemistry,
microbial physiology, and microbial ecology research. Today, WHOI scientists across many departments
employ laboratory studies and field observations to explore and elucidate microbial consortia that (a)
cycle carbon, nutrients and metals in the water column, sediments and bedrock, (b) mediate ecological
relationships in corals, protists and other associations ranging from symbiosis to parasitism, and (c)
influence the health of macro-fauna, from zooplankton to whales. Many of these investigations take
advantage of WHOI’s unique strengths in novel and sophisticated chemical analyses to establish complex
linkages among physiology and genetics with the broader elemental cycling and health of the ocean.
These high-impact studies combine innovative science questions with emerging technologies to generate
novel insights into microbial community organization and function (Table 1). Funding for this work
comes from varied sources, including national funding agencies (NSF, DOE, NOAA, NASA, ONR, NIH)
and private foundations (Gordon and Betty Moore Foundation, Simons Foundation). With deep and broad
expertise, WHOI scientists are uniquely positioned to address transformative questions in ocean
microbiomes, with implications for our understanding of ocean health, resilience and impact on humans.
Areas of Particular Strength. Cultivation and characterization of microbes and associations: Model
organisms are important components of hypothesis testing in microbiome research. Building upon
historical cultivation efforts, WHOI maintains an extensive collection of microbes from diverse marine
environments. Work with these organisms informs an importantly nuanced view of microbial physiology
and its response to a changing environment. Importantly, culture-based physiological experiments enable
the assignment of function to novel genes and proteins, expanding knowledge of metabolic capabilities at
the base of marine food webs and in broader biogeochemical cycling. When expanded to include multiple
species across the three domains of life over both temporal and spatial scales, new insights emerge
regarding the role of geochemical and biological interactions (e.g., symbiosis, parasitism, mutualism) in
microbiome function. By applying advanced microscopy, these interactions can be interrogated in situ to
identify novel microbial functions and their response to, and effect on, their host or surrounding
geochemical environment. The combination of microscopy, cultivation and systems biology provides an
important integrated perspective on the influence of the activity of microorganisms, individually and
collectively, on past, present and future ocean biogeochemistry.
Sampling technologies: Field samples and in situ observations are critically important to establish the
boundaries of microbiome composition and function in their natural setting. Through collaborations
between WHOI scientists and engineers, advanced technologies are uniquely developed at WHOI and
deployed for sampling remote, dynamic marine environments (e.g., hydrothermal vents) at high temporal
and spatial resolution. New platforms are being developed (a) to map microbial populations and their
biogeochemical functions on various scales, including individual whales, time-series stations and ocean
basins, (b) to collect and preserve large-volume samples for advanced chemical and microbial analysis,
(c) to measure in situ metabolic rates, and (d) to conduct in situ incubations at the most realistic
environmental conditions. These technologies reduce sampling artifacts, and will be critical for future
marine microbiome studies that aim to sample extremely labile biomolecules and to estimate in situ
metabolic activity.
Analytical chemistry: Advanced analytical chemistry tools enable microbiome research through the
detection and quantification of biological molecules as well as through the quantification of metabolic
reaction rates. WHOI has played a key role in the innovation of these tools and has unique analytical
capabilities relative to other microbiome research centers. Mass spectrometry-based techniques identify
and quantify biological molecules such as proteins, metabolites and lipids within laboratory and field
studies. These tools complement more common gene-based analyses such as genomics and
transcriptomics with unique perspectives on metabolic reactions. Similarly, WHOI scientists have
developed chemical-sensing technologies that facilitate novel measurements of key metabolites, enabling
a wealth of health and stress-related studies. The chemical tools available at WHOI can now be used to
probe the dynamics of individual metabolic reactions within the context of bulk elemental transformation
rates, thus honing our perspective on global biogeochemistry.
Informatics and data management: Large complex datasets are a blessing (and a curse) of the systems
biology investigations within microbiome research. WHOI has extensive experience in developing tools
for image analysis, for mining mass spectrometry data, and for coupling these complex datasets to
chemical and biological metadata. Often, these tools are broadly applicable to other fields, providing an
opportunity for technology transfer. For example, informatics solutions for automated processing
workflows and web-based data and data product sharing for big data sets of plankton images that were
developed at WHOI are already in use by research groups worldwide. As the home of the Biological and
Chemical Oceanography Data Management Office, WHOI has proven capabilities in data management
and data mining within the ocean sciences, enabling discovery of new insights in historical datasets.
Strengthening WHOI’s Microbiome Research. Ocean microbiome research at WHOI is already strong
and diverse, comprised of a broad collective of scientists and engineers. Nevertheless, we envision a more
cohesive group, well-positioned to take advantage of interdisciplinary funding opportunities at national
agencies and private foundations. Specifically, we want to work together to develop and implement new
tools for sample collection, for in situ measurements and for data integration. WHOI is uniquely strong in
this nexus of science and engineering, but financial barriers currently exist for applying this expertise in
microbiome research. As a first step in increased cohesion and collaboration, we propose the development
of an annual workshop ($25K / year) of microbiome researchers to identify cross-cutting projects.
Support for proof-of-concept projects would be supported by an “Innovation Engine” Fund (~$150K /
year for 3 years). Use of this fund would require a short proposal from at least three investigators
spanning more than one scientific discipline (engineering, biology, chemistry, geology, (geo)physics, data
science), emphasizing the integrative intent of the fund and the focus on technology development. These
new projects would serve as the foundation for new proposals to NSF cross-cutting programs such as the
Science and Technology Centers and/or the Major Research Instrumentation program. Many of the
envisioned cross-cutting projects rely on skilled computational resources. Thus, we request that additional
dedicated funds be used to support a technical staff member who would work jointly among the crosscutting projects. Alternatively, these funds could be used to support a group of existing technical staff
who can work across research groups. We envision that the Institution would support this individual (or
group) fully in the first year, with declining support over 2-3 years as PI support grows. Lastly, student
and postdoc recruitment would be enhanced with a central website ($30K) where research highlights and
opportunities can be posted.
Future Directions. Microbiome research falls squarely within WHOI’s mission, specifically “…to
develop and effectively communicate a fundamental understanding of the processes and characteristics
governing how the oceans function and how they interact with the Earth as a whole.” An Ocean
Microbiome Initiative would support a diverse group of scientists at the Institution and would facilitate
the development of large-scale proposals addressing transformative, challenging questions. Funding for
this initiative would be multi-faceted, expanding relationships with existing funding sources and
facilitating new relationships with donors and philanthropies. The microbiome is a concept familiar to the
educated public and will resonate with a new generation of donors who seek to support basic research in
novel systems. Historically, ocean microbiome research has influenced the medical microbiome sciences
and vice versa, establishing a mutually beneficial conduit of novel scientific insights and innovative
commercial products. Establishing an Ocean Microbiome Initiative at WHOI would nucleate our
scientific staff, administration, and potential donors around a compelling and timely theme, with
implications for improved stewardship of our oceans and the humans, plants and animals that depend on
them. Figure 1. Graphic illustrating the relationship of the “Innovation Engine” concept with various, resulting in enhanced competitive ability for external funds. Table 1. WHOI scientists involved in ocean microbiome research. (*) – leadership team. Name Dept Research focus Anderson, Don BIO Harmful algal blooms Apprill, Amy MCG Marine animal microbiomes Bernhard, Joan MGG Interactions (especially symbioses) and activities Edgcomb, Ginny (*) MGG Genomics, activities and interactions Gast, Rebecca BIO Diversity, symbiosis, parasitism Hahn, Mark BIO Chemical response and adaptation Hansel, Colleen MCG Metabolism, biomineralization Jiang, Huoshou AOPE Engineering solutions to in situ microscopy Johnson, Matt (*) BIO Grazing, mixotrophy Kujawinski, Liz (*) MCG Microbial metabolomics McGillicuddy, Dennis AOPE Mincer, Tracy (*) MCG Microbial chemical interactions Repeta, Dan MCG Microbial nutrient metabolism Saito, Mak MCG Microbial proteomics Sievert, Stefan (*) BIO Diversity, physiology, function, activity Sosik, Heidi BIO Plankton ecology Spivak, Amanda MCG Carbon biogeochemistry, trophic ecology Taylor, Craig BIO Instrumentation, ecology Tarrant, Ann BIO Microbe-­‐‑invertebrate interactions Van Mooy, Ben MCG Lipidomics, phosphorus Wankel, Scott MCG Microbial biogeochemistry