Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores

Sanders, Jon G.; Beichman, Annabel C.; Roman, Joe; Scott, Jarrod J.; Emerson, David; McCarthy, James J.; Girguis, Peter R.

doi:10.1038/ncomms9285

Title: Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores

Journal Article · 21 September 2015 · Nature Communications

DOI: https://doi.org/10.1038/ncomms9285 · OSTI ID:1218871

^[1]; Beichman, Annabel C. ^[2]; Roman, Joe ^[3]; Scott, Jarrod J. ^[4]; Emerson, David ^[4]; McCarthy, James J. ^[1]; Girguis, Peter R. ^[1]

Harvard Univ., Cambridge, MA (United States)
Univ. of California, Los Angeles, CA (United States)
Harvard Univ., Cambridge, MA (United States); Univ. of Vermont, Burlington, VT (United States)
Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)

Mammals host gut microbiomes of immense physiological consequence, but the determinants of diversity in these communities remain poorly understood. Diet appears to be the dominant factor, but host phylogeny also seems to be an important, if unpredictable, correlate. Here we show that baleen whales, which prey on animals (fish and crustaceans), harbor unique gut microbiomes with surprising parallels in functional capacity and higher level taxonomy to those of terrestrial herbivores. These similarities likely reflect a shared role for fermentative metabolisms despite a shift in primary carbon sources from plant-derived to animal-derived polysaccharides, such as chitin. In contrast, protein catabolism and essential amino acid synthesis pathways in baleen whale microbiomes more closely resemble those of terrestrial carnivores. Our results demonstrate that functional attributes of the microbiome can vary independently even given an animal-derived diet, illustrating how diet and evolutionary history combine to shape microbial diversity in the mammalian gut.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1218871

Journal Information:: Nature Communications, Journal Name: Nature Communications Vol. 6; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Taxonomic differences of gut microbiomes drive cellulolytic enzymatic potential within hind-gut fermenting mammals Finlayson-Trick, Emma C. L.; Getz, Landon J.; Slaine, Patrick D. PLOS ONE, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pone.0189404	journal	December 2017
Proteome and microbiota analysis reveals alterations of liver-gut axis under different stocking density of Peking ducks Wu, Yuqin; Li, Jianhui; Qin, Xin PLOS ONE, Vol. 13, Issue 10 https://doi.org/10.1371/journal.pone.0198985	journal	October 2018
Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean Apprill, Amy Frontiers in Marine Science, Vol. 4 https://doi.org/10.3389/fmars.2017.00222	journal	July 2017
Phylogeography and Ecological Niche Shape the Cichlid Fish Gut Microbiota in Central American and African Lakes Baldo, Laura; Riera, Joan Lluís; Salzburger, Walter Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02372	journal	October 2019
Unprecedented Diversity of ssDNA Phages from the Family Microviridae Detected within the Gut of a Protochordate Model Organism (Ciona robusta) Creasy, Alexandria; Rosario, Karyna; Leigh, Brittany Viruses, Vol. 10, Issue 8 https://doi.org/10.3390/v10080404	journal	July 2018
Convergence of gut microbiotas in the adaptive radiations of African cichlid fishes Laura, Baldo,; Lluís, Pretus, Joan; Lluís, Riera, Joan Nature Publishing Group https://doi.org/10.5451/unibas-ep58837	text	January 2017
Geography, seasonality, and host‐associated population structure influence the fecal microbiome of a genetically depauparate Arctic mammal Bird, Samantha; Prewer, Erin; Kutz, Susan Ecology and Evolution, Vol. 9, Issue 23 https://doi.org/10.1002/ece3.5768	journal	November 2019
Characterizing the microbiota in gastrointestinal tract segments of Rhabdophis subminiatus : Dynamic changes and functional predictions Tang, Wenjiao; Zhu, Guangxiang; Shi, Qian MicrobiologyOpen, Vol. 8, Issue 7 https://doi.org/10.1002/mbo3.789	journal	December 2018
Conservation metagenomics: a new branch of conservation biology Wei, Fuwen; Wu, Qi; Hu, Yibo Science China Life Sciences, Vol. 62, Issue 2 https://doi.org/10.1007/s11427-018-9423-3	journal	December 2018
Comparative study on intestinal bacterial communities of Boleophthalmus pectinirostris and Periophthalmus magnuspinnatus with different sexes and feeding strategies Ma, Rongrong; Wang, Sikai; Zhao, Feng Annals of Microbiology, Vol. 68, Issue 3 https://doi.org/10.1007/s13213-018-1324-4	journal	January 2018
Convergence of gut microbiotas in the adaptive radiations of African cichlid fishes Baldo, Laura; Pretus, Joan Lluís; Riera, Joan Lluís The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.62	journal	May 2017
Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea Bik, Elisabeth M.; Costello, Elizabeth K.; Switzer, Alexandra D. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10516	journal	February 2016
Unraveling the processes shaping mammalian gut microbiomes over evolutionary time Groussin, Mathieu; Mazel, Florent; Sanders, Jon G. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14319	journal	February 2017
The life aquatic: advances in marine vertebrate genomics Kelley, Joanna L.; Brown, Anthony P.; Therkildsen, Nina Overgaard Nature Reviews Genetics, Vol. 17, Issue 9 https://doi.org/10.1038/nrg.2016.66	journal	July 2016
Age-associated microbiome shows the giant panda lives on hemicelluloses, not on cellulose Zhang, Wenping; Liu, Wenbin; Hou, Rong The ISME Journal, Vol. 12, Issue 5 https://doi.org/10.1038/s41396-018-0051-y	journal	February 2018
Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes Amato, Katherine R.; G. Sanders, Jon; Song, Se Jin The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0175-0	journal	July 2018
Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome Armstrong, Zachary; Mewis, Keith; Liu, Feng The ISME Journal, Vol. 12, Issue 11 https://doi.org/10.1038/s41396-018-0215-9	journal	July 2018
Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals Perofsky, Amanda C.; Lewis, Rebecca J.; Meyers, Lauren Ancel The ISME Journal, Vol. 13, Issue 1 https://doi.org/10.1038/s41396-018-0251-5	journal	August 2018
Coordinated transformation of the gut microbiome and lipidome of bowhead whales provides novel insights into digestion Miller, Carolyn A.; Holm, Henry C.; Horstmann, Lara The ISME Journal, Vol. 14, Issue 3 https://doi.org/10.1038/s41396-019-0549-y	journal	December 2019
Coordinated change at the colony level in fruit bat fur microbiomes through time Kolodny, Oren; Weinberg, Maya; Reshef, Leah Nature Ecology & Evolution, Vol. 3, Issue 1 https://doi.org/10.1038/s41559-018-0731-z	journal	December 2018
High diversity and unique composition of gut microbiomes in pygmy (Kogia breviceps) and dwarf (K. sima) sperm whales Erwin, Patrick M.; Rhodes, Ryan G.; Kiser, Kevin B. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07425-z	journal	August 2017
Microbial communities in different regions of the gastrointestinal tract in East Asian finless porpoises (Neophocaena asiaeorientalis sunameri) Wan, Xiao-Ling; McLaughlin, Richard William; Zheng, Jin-Song Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-32512-0	journal	September 2018
Dispersal limitation promotes the diversification of the mammalian gut microbiota Moeller, Andrew H.; Suzuki, Taichi A.; Lin, Dana Proceedings of the National Academy of Sciences, Vol. 114, Issue 52 https://doi.org/10.1073/pnas.1700122114	journal	December 2017
Beyond Fermentation: Other Important Services Provided to Endothermic Herbivores by their Gut Microbiota Dearing, M. Denise; Kohl, Kevin D. Integrative and Comparative Biology, Vol. 57, Issue 4 https://doi.org/10.1093/icb/icx020	journal	June 2017
Links between Natural Variation in the Microbiome and Host Fitness in Wild Mammals Suzuki, Taichi A. Integrative and Comparative Biology, Vol. 57, Issue 4 https://doi.org/10.1093/icb/icx104	journal	July 2017
Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association La Reau, Alex J.; Meier-Kolthoff, Jan P.; Suen, Garret Microbial Genomics, Vol. 2, Issue 12 https://doi.org/10.1099/mgen.0.000099	journal	December 2016
Terrestriality and bacterial transfer: A comparative study of gut microbiomes in sympatric Malagasy mammals Perofsky, Amanda C.; Lewis, Rebecca J.; Meyers, Lauren Ancel The ISME Journal https://doi.org/10.1101/293282	journal	April 2018
Proteome and microbiota analysis reveals alterations of liver-gut axis under different stocking density of Peking ducks Wu, Yuqin; Li, Jianhui; Qin, Xin PLOS ONE https://doi.org/10.1101/335570	journal	May 2018
Associations between Afrotropical bats, parasites, and microbial symbionts Lutz Holly, L.; Jackson Elliot, W.; Dick Carl, W. BioRxiv https://doi.org/10.1101/340109	posted_content	September 2018
Effects of host species and environment on the skin microbiome of Plethodontid salamanders Muletz Wolz, Carly R.; Yarwood, Stephanie A.; Campbell Grant, Evan H. Journal of Animal Ecology, Vol. 87, Issue 2 https://doi.org/10.1111/1365-2656.12726	journal	August 2017
Comparison of the gut microbiota of captive common bottlenose dolphins Tursiops truncatus in three aquaria Suzuki, A.; Segawa, T.; Sawa, S. Journal of Applied Microbiology, Vol. 126, Issue 1 https://doi.org/10.1111/jam.14109	journal	October 2018
Rates of gut microbiome divergence in mammals Nishida, Alex H.; Ochman, Howard Molecular Ecology, Vol. 27, Issue 8 https://doi.org/10.1111/mec.14473	journal	January 2018
Stable isotope analysis of fecal material provides insight into the diet of fin whales Arregui, Marina; Borrell, Asunción; Víkingsson, Gisli Marine Mammal Science, Vol. 34, Issue 4 https://doi.org/10.1111/mms.12504	journal	March 2018
Dynamic microbiome evolution in social bees Kwong, Waldan K.; Medina, Luis A.; Koch, Hauke Science Advances, Vol. 3, Issue 3 https://doi.org/10.1126/sciadv.1600513	journal	March 2017
Chitinase genes ( CHIA s) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals Emerling, Christopher A.; Delsuc, Frédéric; Nachman, Michael W. Science Advances, Vol. 4, Issue 5 https://doi.org/10.1126/sciadv.aar6478	journal	May 2018
Temporal and Regional Variability in the Skin Microbiome of Humpback Whales along the Western Antarctic Peninsula Bierlich, K. C.; Miller, Carolyn; DeForce, Emelia Applied and Environmental Microbiology, Vol. 84, Issue 5 https://doi.org/10.1128/aem.02574-17	journal	December 2017
Allometry and Ecology of the Bilaterian Gut Microbiome Sherrill-Mix, Scott; McCormick, Kevin; Lauder, Abigail mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mbio.00319-18	journal	March 2018
Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats Song, Se Jin; Sanders, Jon G.; Delsuc, Frédéric mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mbio.02901-19	journal	January 2020
Experimental Evidence for Adaptation to Species-Specific Gut Microbiota in House Mice Moeller, Andrew H.; Gomes-Neto, João C.; Mantz, Sara mSphere, Vol. 4, Issue 4 https://doi.org/10.1128/msphere.00387-19	journal	July 2019
Ecology and Host Identity Outweigh Evolutionary History in Shaping the Bat Microbiome Lutz, Holly L.; Jackson, Elliot W.; Webala, Paul W. mSystems, Vol. 4, Issue 6 https://doi.org/10.1128/msystems.00511-19	journal	November 2019
The human microbiome in evolution Davenport, Emily R.; Sanders, Jon G.; Song, Se Jin BMC Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12915-017-0454-7	journal	December 2017
Tiny microbes, enormous impacts: what matters in gut microbiome studies? Debelius, Justine; Song, Se Jin; Vazquez-Baeza, Yoshiki Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1086-x	journal	October 2016
Skin microbiome of coral reef fish is highly variable and driven by host phylogeny and diet Chiarello, Marlène; Auguet, Jean-Christophe; Bettarel, Yvan Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0530-4	journal	August 2018
The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch Michel, Alice J.; Ward, Lewis M.; Goffredi, Shana K. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0555-8	journal	September 2018
The Brain of the Domestic Bos taurus: Weight, Encephalization and Cerebellar Quotients, and Comparison with Other Domestic and Wild Cetartiodactyla Ballarin, Cristina; Povinelli, Michele; Granato, Alberto PLOS ONE, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pone.0154580	journal	April 2016
Proteome and microbiota analysis reveals alterations of liver-gut axis under different stocking density of Peking ducks Wu, Yuqin; Li, Jianhui; Qin, Xin PLOS ONE, Vol. 13, Issue 10 https://doi.org/10.1371/journal.pone.0198985	journal	October 2018
The Pacific harbor seal gut microbiota in Mexico: Its relationship with diet and functional inferences Pacheco-Sandoval, Arlette; Schramm, Yolanda; Heckel, Gisela PLOS ONE, Vol. 14, Issue 8 https://doi.org/10.1371/journal.pone.0221770	journal	August 2019
The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch Michel, Alice J.; Ward, Lewis M.; Goffredi, Shana K. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.27737	collection	January 2018
Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean Apprill, Amy Frontiers in Marine Science, Vol. 4 https://doi.org/10.3389/fmars.2017.00222	journal	July 2017
Beyond 16S rRNA Community Profiling: Intra-Species Diversity in the Gut Microbiota Ellegaard, Kirsten M.; Engel, Philipp Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01475	journal	September 2016
Metagenomic Study Suggests That the Gut Microbiota of the Giant Panda (Ailuropoda melanoleuca) May Not Be Specialized for Fiber Fermentation Guo, Wei; Mishra, Sudhanshu; Zhao, Jiangchao Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00229	journal	February 2018
Comparing Microbiome Sampling Methods in a Wild Mammal: Fecal and Intestinal Samples Record Different Signals of Host Ecology, Evolution Ingala, Melissa R.; Simmons, Nancy B.; Wultsch, Claudia Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00803	journal	May 2018
Unprecedented Diversity of ssDNA Phages from the Family Microviridae Detected within the Gut of a Protochordate Model Organism (Ciona robusta) Creasy, Alexandria; Rosario, Karyna; Leigh, Brittany Viruses, Vol. 10, Issue 8 https://doi.org/10.3390/v10080404	journal	July 2018
Convergence of gut microbiotas in the adaptive radiations of African cichlid fishes Laura, Baldo,; Lluís, Pretus, Joan; Lluís, Riera, Joan Nature Publishing Group https://doi.org/10.5451/unibas-ep58837	text	January 2017
A survey of the sperm whale ( Physeter catodon ) commensal microbiome Li, Chang; Tan, Xiaoxuan; Bai, Jie PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7257	journal	January 2019

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