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      Extensive Core Microbiome in Drone-Captured Whale Blow Supports a Framework for Health Monitoring

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          Abstract

          The conservation and management of large whales rely in part upon health monitoring of individuals and populations, and methods generally necessitate invasive sampling. Here, we used a small, unmanned hexacopter drone to noninvasively fly above humpback whales from two populations, capture their exhaled breath (blow), and examine the associated microbiome. In the first extensive examination of the large-whale blow microbiome, we present surprising results about the discovery of a large core microbiome that was shared across individual whales from geographically separated populations in two ocean basins. We suggest that this core microbiome, in addition to other microbiome characteristics, could be a useful feature for health monitoring of large whales worldwide.

          ABSTRACT

          The pulmonary system is a common site for bacterial infections in cetaceans, but very little is known about their respiratory microbiome. We used a small, unmanned hexacopter to collect exhaled breath condensate (blow) from two geographically distinct populations of apparently healthy humpback whales ( Megaptera novaeangliae), sampled in the Massachusetts coastal waters off Cape Cod ( n = 17) and coastal waters around Vancouver Island ( n = 9). Bacterial and archaeal small-subunit rRNA genes were amplified and sequenced from blow samples, including many of sparse volume, as well as seawater and other controls, to characterize the associated microbial community. The blow microbiomes were distinct from the seawater microbiomes and included 25 phylogenetically diverse bacteria common to all sampled whales. This core assemblage comprised on average 36% of the microbiome, making it one of the more consistent animal microbiomes studied to date. The closest phylogenetic relatives of 20 of these core microbes were previously detected in marine mammals, suggesting that this core microbiome assemblage is specialized for marine mammals and may indicate a healthy, noninfected pulmonary system. Pathogen screening was conducted on the microbiomes at the genus level, which showed that all blow and few seawater microbiomes contained relatives of bacterial pathogens; no known cetacean respiratory pathogens were detected in the blow. Overall, the discovery of a shared large core microbiome in humpback whales is an important advancement for health and disease monitoring of this species and of other large whales.

          IMPORTANCE The conservation and management of large whales rely in part upon health monitoring of individuals and populations, and methods generally necessitate invasive sampling. Here, we used a small, unmanned hexacopter drone to noninvasively fly above humpback whales from two populations, capture their exhaled breath (blow), and examine the associated microbiome. In the first extensive examination of the large-whale blow microbiome, we present surprising results about the discovery of a large core microbiome that was shared across individual whales from geographically separated populations in two ocean basins. We suggest that this core microbiome, in addition to other microbiome characteristics, could be a useful feature for health monitoring of large whales worldwide.

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          SAR11 clade dominates ocean surface bacterioplankton communities.

          The most abundant class of bacterial ribosomal RNA genes detected in seawater DNA by gene cloning belongs to SAR11-an alpha-proteobacterial clade. Other than indications of their prevalence in seawater, little is known about these organisms. Here we report quantitative measurements of the cellular abundance of the SAR11 clade in northwestern Sargasso Sea waters to 3,000 m and in Oregon coastal surface waters. On average, the SAR11 clade accounts for a third of the cells present in surface waters and nearly a fifth of the cells present in the mesopelagic zone. In some regions, members of the SAR11 clade represent as much as 50% of the total surface microbial community and 25% of the subeuphotic microbial community. By extrapolation, we estimate that globally there are 2.4 x 10(28) SAR11 cells in the oceans, half of which are located in the euphotic zone. Although the biogeochemical role of the SAR11 clade remains uncertain, these data support the conclusion that this microbial group is among the most successful organisms on Earth.
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            Optimizing methods and dodging pitfalls in microbiome research

            Research on the human microbiome has yielded numerous insights into health and disease, but also has resulted in a wealth of experimental artifacts. Here, we present suggestions for optimizing experimental design and avoiding known pitfalls, organized in the typical order in which studies are carried out. We first review best practices in experimental design and introduce common confounders such as age, diet, antibiotic use, pet ownership, longitudinal instability, and microbial sharing during cohousing in animal studies. Typically, samples will need to be stored, so we provide data on best practices for several sample types. We then discuss design and analysis of positive and negative controls, which should always be run with experimental samples. We introduce a convenient set of non-biological DNA sequences that can be useful as positive controls for high-volume analysis. Careful analysis of negative and positive controls is particularly important in studies of samples with low microbial biomass, where contamination can comprise most or all of a sample. Lastly, we summarize approaches to enhancing experimental robustness by careful control of multiple comparisons and to comparing discovery and validation cohorts. We hope the experimental tactics summarized here will help researchers in this exciting field advance their studies efficiently while avoiding errors. Electronic supplementary material The online version of this article (doi:10.1186/s40168-017-0267-5) contains supplementary material, which is available to authorized users.
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              The role of the bacterial microbiome in lung disease.

              Novel culture-independent techniques have recently demonstrated that the lower respiratory tract, historically considered sterile in health, contains diverse communities of microbes: the lung microbiome. Increasing evidence supports the concept that a distinct microbiota of the lower respiratory tract is present both in health and in various respiratory diseases, although the biological and clinical significance of these findings remains undetermined. In this article, the authors review and synthesize published reports of the lung microbiota of healthy and diseased subjects, discuss trends of microbial diversity and constitution across disease states, and look to the extrapulmonary microbiome for hypotheses and future directions for study.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                10 October 2017
                Sep-Oct 2017
                : 2
                : 5
                : e00119-17
                Affiliations
                [a ]Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA
                [b ]Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA
                [c ]Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA, La Jolla, California, USA
                [d ]SR 3 SeaLife Response, Rehabilitation, and Research, Mukilteo, Washington, USA
                [e ]Coastal Ocean Research Institute, Vancouver Aquarium, Vancouver, BC, Canada
                [f ]Zoology Department, University of British Columbia, Vancouver, BC, Canada
                Northern Arizona University
                Author notes
                Address correspondence to Amy Apprill, aapprill@ 123456whoi.edu .

                A.A. and C.A.M. contributed equally to this work.

                Citation Apprill A, Miller CA, Moore MJ, Durban JW, Fearnbach H, Barrett-Lennard LG. 2017. Extensive core microbiome in drone-captured whale blow supports a framework for health monitoring. mSystems 2:e00119-17. https://doi.org/10.1128/mSystems.00119-17.

                Author information
                http://orcid.org/0000-0002-4249-2977
                Article
                mSystems00119-17
                10.1128/mSystems.00119-17
                5634792
                29034331
                3190d954-e72f-4f1f-9dfb-4bbb1593b80a
                Copyright © 2017 Apprill et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 5 September 2017
                : 13 September 2017
                Page count
                supplementary-material: 3, Figures: 6, Tables: 2, Equations: 0, References: 57, Pages: 15, Words: 8787
                Funding
                Funded by: Woods Hole Oceanographic Institution (WHOI) https://doi.org/10.13039/100005991
                Award ID: Ocean Life Institute
                Award Recipient : Amy Apprill Award Recipient : Michael Moore Award Recipient : John Durban
                Categories
                Research Article
                Host-Microbe Biology
                Custom metadata
                September/October 2017

                ssu rrna gene,bacteria,drone,humpback whale,microbiome
                ssu rrna gene, bacteria, drone, humpback whale, microbiome

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