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Synergy among Microbiota and Their Hosts: Leveraging the Hawaiian Archipelago and Local Collaborative Networks To Address Pressing Questions in Microbiome Research


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Despite increasing acknowledgment that microorganisms underpin the healthy functioning of basically all multicellular life, few cross-disciplinary teams address the diversity and function of microbiota across organisms and ecosystems. Our newly formed consortium of junior faculty spanning fields such as ecology and geoscience to mathematics and molecular biology from the University of Hawai‘i at Mānoa aims to fill this gap. We are united in our mutual interest in advancing a new paradigm for biology that incorporates our modern understanding of the importance of microorganisms. As our first concerted research effort, we will assess the diversity and function of microbes across an entire watershed on the island of Oahu, Hawai‘i. Due to its high ecological diversity across tractable areas of land and sea, Hawai‘i provides a model system for the study of complex microbial communities and the processes they mediate. Owing to our diverse expertise, we will leverage this study system to advance the field of biology.
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Synergy among Microbiota and Their Hosts: Leveraging the
Hawaiian Archipelago and Local Collaborative Networks To
Address Pressing Questions in Microbiome Research
Nicole A. Hynson,
Kiana L. Frank,
Rosanna A. Alegado,
Anthony S. Amend,
Mohammad Arif,
Gordon M. Bennett,
Andrea J. Jani,
Matthew C. I. Medeiros,
Yuriy Mileyko,
Craig E. Nelson,
Nhu H. Nguyen,
Olivia D. Nigro,
Sladjana Prisic,
Sangwoo Shin,
Daisuke Takagi,
Samuel T. Wilson,
Joanne Y. Yew
Department of Botany, University of Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
Pacific Biosciences Research Center, University of Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
Center for Microbial Oceanography: Research and Education, Department of Oceanography, University of
Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
Department of Plant and Environmental Protection Sciences, University of Hawai‘i at Manoa, Honolulu,
Hawai‘i, USA
Department of Mathematics, University of Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
Sea Grant College Program, University of Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
Department of Tropical Plant and Soil Sciences, University of Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
Department of Microbiology, University of Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
Department of Mechanical Engineering, University of Hawai‘i at Manoa, Honolulu, Hawai‘i, USA
ABSTRACT Despite increasing acknowledgment that microorganisms underpin the
healthy functioning of basically all multicellular life, few cross-disciplinary teams ad-
dress the diversity and function of microbiota across organisms and ecosystems. Our
newly formed consortium of junior faculty spanning fields such as ecology and geo-
science to mathematics and molecular biology from the University of Hawai‘i at
Manoa aims to fill this gap. We are united in our mutual interest in advancing a new
paradigm for biology that incorporates our modern understanding of the impor-
tance of microorganisms. As our first concerted research effort, we will assess the di-
versity and function of microbes across an entire watershed on the island of Oahu,
Hawai‘i. Due to its high ecological diversity across tractable areas of land and sea,
Hawai‘i provides a model system for the study of complex microbial communities
and the processes they mediate. Owing to our diverse expertise, we will leverage
this study system to advance the field of biology.
KEYWORDS ecology, environmental microbiology, evolution, microbiome, paradigm
Crucial to science is understanding whether it is itself reductionist: do first principles
from one field, such as physics, explain the fundaments of others like molecular
biology? The answer to this question hinges upon whether scientists speak the same
language. Consortia that link multiple scientific fields offer the powerful promise of
extending any single individual’s research to a more globally unifying endeavor. We see
this as one of the potential primary outcomes of our newly established collaboration of
junior faculty, the Center for Microbiome Analysis through Island Knowledge and
Investigation (C-MAIKI). By overcoming the technical and philosophical barriers that
often silo disparate disciplines, our goal is to advance the field of microbial systems
biology. We are a diverse group of early career researchers from the University of
Hawai‘i at Manoa who are fascinated by the microbial world. Our individual research
programs span natural environments, including sea, land, and freshwater, as well as
Received 30 October 2017 Accepted 28
November 2017 Published 13 March 2018
Citation Hynson NA, Frank KL, Alegado RA,
Amend AS, Arif M, Bennett GM, Jani AJ,
Medeiros MCI, Mileyko Y, Nelson CE, Nguyen
NH, Nigro OD, Prisic S, Shin S, Takagi D, Wilson
ST, Yew JY. 2018. Synergy among microbiota
and their hosts: leveraging the Hawaiian
archipelago and local collaborative networks to
address pressing questions in microbiome
research. mSystems 3:e00159-17. https://doi
Copyright © 2018 Hynson et al. This is an
open-access article distributed under the terms
of the Creative Commons Attribution 4.0
International license.
Address correspondence to Nicole A. Hynson,
Conflict of Interest Disclosures: N.A.H. has
nothing to disclose. K.L.F. has nothing to
disclose. R.A.A. has nothing to disclose. A.S.A.
has nothing to disclose. M.A. has nothing to
disclose. G.M.B. has nothing to disclose. A.J.J.
has nothing to disclose. M.C.I.M. has nothing to
disclose. Y.M. has nothing to disclose. C.E.N.
reports grant OCE-1538393 from the U.S.
National Science Foundation and grant
NA14OAR4170071 from the National Oceanic
and Atmospheric Administration during the
conduct of the study. N.H.N. has nothing to
disclose. O.D.N. has nothing to disclose. S.P.
received grants NIH-NIAID R21 AI109293, HCF–
Leahi Fund–17ADVC-86185, and NIH-NIGMS
P30 GM114737 during the conduct of the
study. S.S. has nothing to disclose. D.T. has
nothing to disclose. S.T.W. has nothing to
disclose. J.Y.Y. has nothing to disclose.
mSystems® vol. 3, no. 2, is a special issue
sponsored by Janssen Human Microbiome
Institute (JHMI).
Ecological and Evolutionary Science
March/April 2018 Volume 3 Issue 2 e00159-17 1
model laboratory systems, such as fruit flies and rodents, while our study organisms
range from viruses, bacteria, protists, and fungi to plants and animals, including
humans (1–6). Some of us are not even biologists in the traditional sense, but rather
mechanical engineers and mathematicians who look to nature to understand and
create complex systems (7–9). Together, we seek to illuminate the diversity and
function of microbes within Hawaiian ecosystems to examine whether their roles are
conserved across hosts and environments and the extent to which disturbances alter
the functioning of microbially mediated processes.
While concepts such as keystone species, ecosystem engineers, and diversity/
productivity relationships have been well documented for many macroorganisms, our
knowledge of these features of microbial communities is limited. Three of the persistent
challenges to assessing the ecology of microbes have been (i) ascribing meaningful
taxonomic units that can be used to test evolutionary and ecological theories, (ii)
disentangling the relative contributions of evolutionary and ecological processes to the
community assembly and function of microbes, and (iii) understanding the spatial and
temporal scales that are relevant for microbial interactions and the processes they
mediate (10). Given the ever-increasing amounts of genomic data that can be used to
determine the identity of microbes and the fact that evolutionary and population
genetics theories provide fundamental frameworks for examining ecological patterns,
solving the first two challenges seem relatively close at hand: it is just a matter of
choosing a biological scale that is relevant for microbes (that is, what is the appropriate
unit of selection for microorganisms?). Thus, we see the third challenge— deriving the
appropriate space-time scales for the study of microbes, their interactions with each
other, and their environments—as the most critical. We intend to make the most
progress toward addressing this challenge in the years to come.
With our collective recognition that microbes underpin the healthy function of all
multicellular life, we have come together to take a multifaceted approach to bridging
two vast knowledge gaps in the quickly growing field of microbiome research: which
environments act as reservoirs for symbiotic microbes when they are outside the host,
and how we can manage our environments to promote and maintain healthy microbial
partnerships? We are uniquely positioned to address these questions due to our diverse
and complementary expertise, as well as our location on the island of O’ahu in the
Hawaiian archipelago. Hawai‘i has long been recognized by climatologists, ecologists,
and evolutionary biologists as a model system for the study of natural phenomena.
While covering only 0.004% of the Earth’s total land area (similar to the size of
Massachusetts), over a matter of kilometers, Hawaiian bioregions contain comparable
environmental diversity to that typically found on much larger spatial scales, like
continents. For example, Hawai‘i has a rainfall gradient from 204 mm/year on average
near the summit of Mauna Kea (similar to averages in the Gobi Desert in Asia), to
10,271 mm/year on average on the slopes of Haleakala(similar to parts of the
Chocó-Darién, Columbia, one of the wettest places on Earth). Because Hawai‘i is one of
the most remote island chains on Earth, non-human-assisted dispersal is a significant
hurdle for the establishment of most organisms. As a result, Hawai‘i’s macrobiota is
90% endemic, with well-known evolutionary histories. While far less is known about
the diversity of Hawai‘i’s microbes, evidence from recent surveys suggests that its
microbial communities are dominated by taxa, at least to the generic level, found
throughout the world (11, 12). For example, a recent study of phyllosphere fungi
associated with a single genus of endemic Hawaiian plant Clermontia revealed that
communities are hyperdiverse, harboring thousands of fungal operational taxonomic
units (species equivalents). This result is similar to the findings of a global assessment
of foliar fungal endophytes where tropical ecosystems harbored the greatest relative
diversity (12, 13). Thus, Hawai‘i is a relatively small and closed system, with suites of
March/April 2018 Volume 3 Issue 2 e00159-17 2
environmental conditions similar to those found throughout the globe, and is occupied
by many of the same guilds of microorganisms also found elsewhere. We have the ideal
“living laboratory” for the study of microbiota and microbially mediated processes.
While prior research on microbiomes has focused on changes in microbial diversity
across various environmental conditions in single hosts, we now recognize the con-
nectivity across habitats and hosts and the microbial “neighborhood” as critical drivers
of community composition (14)(Fig. 1). Through broad-scale sampling, we have
identified traits and taxonomy that predict nonrandom overlap of microbial community
members across disparate hosts and habitats (15, 16). For example, fungi in the genus
Malassezia have been identified as numerically dominant in most marine systems
examined throughout the Hawaiian Archipelago, yet some of the same genotypes
appear in soil, plant, and even air samples (11). Also, studies on Hawaiian insect-
microbe interactions have revealed that many host taxa selectively harbor distinct
microbial communities, some of which appear to be intrinsic to hosts’ use of environ-
mental resources and underpin their adaptation to Hawai‘i’s diverse environments (19).
This connectivity begs the following questions: what habitat(s) represent the regional
species pool, and are there conserved functions of these shared microbes across hosts
and habitats?
As a next step to elucidate the mechanisms underlying these patterns of connec-
tivity, we plan to assess the community dynamics of microbes as they transition from
free-living to symbiotic states across an entire watershed, including the macrobiota
living in it, that spans mountain ridges to fringing coral reef habitats (Fig. 1). Using a
diversity of -omic approaches, as well as assays such as extracellular enzyme and lipid
production to assess microbial functional traits, we will determine the identity and
functional flexibility of microbes across hosts and habitats and how this impacts host
FIG 1 Conceptual schematic of C-MAIKI’s approach to address pressing questions in microbiome research by evaluating synergy (red arrows) among
environmental microbiota and their hosts—from free-living to symbiotic lifestyles—leveraging the unique and replicable gradients across Hawaiian water-
sheds—from mountain (terrestrial) to sea (marine) habitats. Recognizing that microbes underpin the healthy function of all multicellular life, this synergistic
cross-disciplinary approach allows us to address what environments act as reservoirs for symbiotic microbes when they are outside the host and how we can
manage our environments to promote and maintain healthy microbial partnerships.
March/April 2018 Volume 3 Issue 2 e00159-17 3
and environmental health. Through manipulative field and laboratory experiments
within and outside hosts and across steep environmental gradients, we will then test
the resilience of microbial communities to perturbations in their living conditions.
These data will provide the training ground for predictive probabilistic models that
identify how we may manipulate microbial communities to restore or elicit specific host
functions or ecosystem states. Using population genomic approaches combined with
classic tools from population genetics and coalescent theory, we hope to advance our
understanding of microbial migration and source-sink relationships for microbes, in-
cluding how transitions from drastically different environments (e.g., terrestrial to
marine) or hosts (e.g., corals to insects) are made.
Over the next 5 years, the field of microbiology has much to contribute, as well as
much to learn, from the broader scientific community and disciplines. In the same vein
as Thomas Kuhn’s The Structure of Scientific Revolutions (17), we would argue that the
field of biology, until fairly recently, was in a stage of “normal science” where our
interest in, and understanding of, the microbial world had been observed through
the lens of macrobiology. Brought on by the immense technological innovations in
DNA sequencing, we are shining a bright floodlight on the previously hidden world
of microbes and its fundamental role in shaping ecosystems across all trophic levels.
We are now in the early stages of a paradigm shift, the boundaries of which are only
beginning to be delineated. In the years to come, we anticipate this paradigm shift
being fueled by novel technologies and their ease of use, such as single-molecule
sequencing, single-cell sorting from environmental communities, and increasingly
streamlined computational platforms for large data sets. However, for this shift to
become fully realized, it will not only require that we integrate microbes into
(macro)biological concepts, but that we create new theories, models, and collab-
orations. As a cohort, the C-MAIKI faculty envisions the development of a new
framework for biology that leverages our study system and our cross-disciplinary
interactions to lay this new foundation.
On the flip side of reductionism is synergism, or the concept popularized by the field
of ecology, that the additive effects of interacting organisms result in something more
than the sum of their individual constituents. The classic example of synergism is the
significant and positive relationship between plant diversity and primary productivity
(18). While the cause for such synergism even among well-studied macroorganisms still
remains somewhat elusive, our research endeavors will shed new light on the emergent
properties of microbiomes. For example, collaborations among those of us who focus
on model systems and those who work in field settings can transform our understand-
ing of basic physiological and evolutionary processes. By using well-studied organisms
such as Drosophila spp. in manipulative field experiments, we can elucidate the
molecular mechanisms by which environmental microbes alter the physiology and
phenotype of their hosts. Our collaborations will not only build a means for cross-
communication among disciplines, perhaps revealing the reductionist side of micro-
biomes, but they will also result in synergistic breakthroughs that allow us to answer
some of the most pertinent questions in the life sciences.
We thank the Office of the Vice Chancellor for Research at the University of Hawai‘i
at Manoa for funding. This paper is funded in part by a grant/cooperative agreement
from the National Oceanic and Atmospheric Administration (NOAA), project R/WR-3,
which is sponsored by the University of Hawai‘i Sea Grant College Program, SOEST,
under institutional grant no. NA14OAR4170071 from NOAA’s National Sea Grant Office,
Department of Commerce.
March/April 2018 Volume 3 Issue 2 e00159-17 4
The views expressed herein are those of the authors and do not necessarily reflect
the views of NOAA or any of its subagencies.
This is publication number 10279 of the School of Ocean and Earth Science and
Technology of the University of Hawai‘i at Manoa and publication UNIHI-SEAGRANT-
JC-16-13 of the University of Hawai‘i Sea Grant College Program.
1. Bennett GM, Moran NA. 2015. Heritable symbiosis: the advantages and
perils of an evolutionary rabbit hole. Proc Natl Acad Sci U S A 112:
10169 –10176.
2. Prisic S, Hwang H, Dow A, Barnaby O, Pan TS, Lonzanida JA, Chazin WJ,
Steen H, Husson RN. 2015. Zinc regulates a switch between primary and
alternative S18 ribosomal proteins in Mycobacterium tuberculosis. Mol
Microbiol 97:263–280.
3. Medeiros MC, Anderson TK, Higashiguchi JM, Kitron UD, Walker ED,
Brawn JD, Krebs BL, Ruiz MO, Goldberg TL, Ricklefs RE, Hamer GL. 2014.
An inverse association between West Nile virus serostatus and avian
malaria infection status. Parasit Vectors 7:415.
4. Nigro OD, Jungbluth SP, Lin HT, Hsieh CC, Miranda JA, Schvarcz CR,
Rappé MS, Steward GF. 2017. Viruses in the oceanic basement. mBio
5. Sogin EM, Putnam HM, Nelson CE, Anderson P, Gates RD. 2017. Corre-
spondence of coral holobiont metabolome with symbiotic bacteria,
archaea and Symbiodinium communities. Environ Microbiol Rep
9:310 –315.
6. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K,
King N. 2011. Cell differentiation and morphogenesis in the colony-
forming choanoflagellate Salpingoeca rosetta. Dev Biol 357:73– 82.
7. Weitz JS, Mileyko Y, Joh RI, Voit EO. 2008. Collective decision making in
bacterial viruses. Biophys J 95:2673–2680.
8. Takagi D, Braunschweig AB, Zhang J, Shelley MJ. 2013. Dispersion of
self-propelled rods undergoing fluctuation-driven flips. Phys Rev Lett
9. Shin S, Um E, Sabass B, Ault JT, Rahimi M, Warren PB, Stone HA. 2016.
Size-dependent control of colloid transport via solute gradients in dead-
end channels. Proc Natl Acad SciUSA113:257–261.
10. Hynson NA. 2014. Fungal ecology beyond boundaries: from communi-
ties to the globe. Fungal Ecol 12:1–3.
11. Amend A. 2014. From dandruff to deep-sea vents: Malassezia-like fungi
are ecologically hyper-diverse. PLoS Pathog 10:e1004277. https://doi
12. Datlof EM, Amend AS, Earl K, Hayward J, Morden CW, Wade R, Zahn G,
Hynson NA. 2017. Uncovering unseen fungal diversity from plant DNA
banks. PeerJ 5:e3730.
13. Arnold AE, Lutzoni F. 2007. Diversity and host range of foliar fungal
endophytes: are tropical leaves biodiversity hotspots? Ecology 88:
14. Haas AF, Fairoz MFM, Kelly LW, Nelson CE, Dinsdale EA, Edwards RA,
Giles S, Hatay M, Hisakawa N, Knowles B, Lim YW, Maughan H, Pantos O,
Roach TNF, Sanchez SE, Silveira CB, Sandin S, Smith JE, Rohwer F. 2016.
Global microbialization of coral reefs. Nat Microbiol 1:16042. https://doi
15. Jani AJ, Knapp RA, Briggs CJ. 2017. Epidemic and endemic pathogen
dynamics correspond to distinct host population microbiomes at a
landscape scale. Proc R Soc B 284:20170944.
16. Wainwright BJ, Zahn GL, Spalding HL, Sherwood AR, Smith CM, Amend
AS. 2017. Fungi associated with mesophotic macroalgae from the ‘Au’Au
Channel, west Maui are differentiated by host and overlap terrestrial
communities. PeerJ 5:e3532.
17. Kuhn TS. 2012. The structure of scientific revolutions, 4th ed. University
of Chicago Press, Chicago, IL.
18. Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E. 1997. The
influence of functional diversity and composition on ecosystem processes.
Science 277:1300 –1302.
19. Poff KE, Stever H, Reil JB, Seabourn P, Ching AJ, Aoki S, Logan M,
Michalski JR, Santamaria J, Adams JW, Eiben JA, Yew JY, Ewing CP,
Magnacca KN, Bennett GM. 2017. The native Hawaiian insect micro-
biome initiative: a critical perspective for Hawaiian insect evolution.
Insects 8:130.
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... The first C-MAIKI (Center for Microbiome Analysis through Island Knowledge and Investigation) project was formed by an interdisciplinary consortium of faculty at the University of Hawai'i at Mānoa to assess the diversity and function of microbes across an entire watershed on the island of Oahu, Hawai'i (Hynson et al. 2018). The portion of the project concerning this research is described below. ...
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Significance Dead-end geometries are commonly found in many porous systems. Particle transport into such dead-end pores is often important, but is difficult to achieve owing to the confinement. It is natural to expect that Brownian motion is the sole mechanism to deliver the particles into the pores, but that mechanism is, unfortunately, slow and inefficient. Here, we introduce solute gradient to control the transport of particles in dead-end channels. We demonstrate a size effect such that larger particles tend to focus more and reside deeper in the channels. Our findings suggest a potential pathway to many useful applications that are difficult to achieve in dead-end geometries such as particle sorting and sample preconcentration, which are important in pharmaceuticals and healthcare industries.
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The Mycobacterium tuberculosis genome encodes five putative "alternative" ribosomal proteins whose expression is repressed at high Zn(2+) concentration. Each alternative protein has a primary homolog that is predicted to bind Zn(2+) . We hypothesized that zinc triggers a switch between these paired homologous proteins and therefore chose one of these pairs, S18-1/S18-2, to study mechanisms of the predicted competition for their incorporation into ribosomes. As predicted, our data show that Zn(2+) -depletion causes accumulation of both S18-2 mRNA and protein. In contrast, S18-1 mRNA levels are unchanged to slightly elevated under Zn(2+) -limited conditions. However the amount of S18-1 protein is markedly decreased. We further demonstrate that both S18 proteins interact with ribosomal protein S6, a committed step in ribosome biogenesis. Zn(2+) is absolutely required for the S18-1/S6 interaction, while it is dispensable for S18-2/S6 dimer formation. These data suggest a model in which the S18-1 is the dominant ribosome constituent in high zinc conditions, e.g. inside of phagosomes, but that it can be replaced by S18-2 when zinc is deficient, e.g. in the extracellular milieu. Consequently, Zn(2+) -depletion may serve as a signal for building alternative ribosomes when M. tuberculosis is released from macrophages, to allow survival in the extracellular environment. This article is protected by copyright. All rights reserved.
Microbial symbiotic partners, such as those associated with scleractinian corals, mediate biochemical transformations that influence host performance and survival. While evidence suggests microbial community composition partly accounts for differences in coral physiology, how these symbionts affect metabolic pathways remains underexplored. We aimed to assess functional implications of variation among coral-associated microbial partners in hospite. To this end, we characterized and compared metabolomic profiles and microbial community composition from nine reef-building coral species. These data demonstrate metabolite profiles and microbial communities are species-specific and are correlated to one another. Using Porites spp. as a case study, we present evidence that the relative abundance of different sub-clades of Symbiodinium and bacterial/archaeal families are linked to positive and negative metabolomic signatures. Our data suggests that while some microbial partners benefit the union, others are more opportunistic with potential detriment to the host. Consequently, coral partner choice likely influences cellular metabolic activities and, therefore, holobiont nutrition. This article is protected by copyright. All rights reserved.
Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sap-feeding insects, and Buchnera aphidicola, a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the host-symbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing host-pathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphid-Buchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.