ORIGINAL RESEARCH published: 01 April 2021 doi: 10.3389/fmars.2021.627724 Edited by: Andrew Stanley Mount, Clemson University, United States Reviewed by: John HR Burns, University of Hawaii at Hilo, United States Sebastian Fraune, Heinrich Heine University of Düsseldorf, Germany *Correspondence: Mark Little marklittle1989@gmail.com Ty N. F. Roach smokinroachjr@gmail.com † These authors have contributed equally to this work and share first authorship Specialty section: This article was submitted to Marine Molecular Biology and Ecology, a section of the journal Frontiers in Marine Science Received: 10 November 2020 Accepted: 02 February 2021 Published: 01 April 2021 Citation: Little M, George EE, Arts MGI, Shivak J, Benler S, Huckeba J, Quinlan ZA, Boscaro V, Mueller B, Güemes AGC, Rojas MI, White B, Petras D, Silveira CB, Haas AF, Kelly LW, Vermeij MJA, Quinn RA, Keeling PJ, Dorrestein PC, Rohwer F and Roach TNF (2021) Three-Dimensional Molecular Cartography of the Caribbean Reef-Building Coral Orbicella faveolata. Front. Mar. Sci. 8:627724. doi: 10.3389/fmars.2021.627724 Three-Dimensional Molecular Cartography of the Caribbean Reef-Building Coral Orbicella faveolata Mark Little 1,2 * † , Emma E. George 3† , Milou G. I. Arts 4,5 , Jade Shivak 3 , Sean Benler 6 , Joel Huckeba 7 , Zachary A. Quinlan 1,2 , Vittorio Boscaro 3 , Benjamin Mueller 8,9 , Ana Georgina Cobián Güemes 10 , Maria Isabel Rojas 1,2 , Brandie White 1,2 , Daniel Petras 11 , Cynthia B. Silveira 12 , Andreas F. Haas 4 , Linda Wegley Kelly 1,2 , Mark J. A. Vermeij 8,9 , Robert A. Quinn 13 , Patrick J. Keeling 3 , Pieter C. Dorrestein 11 , Forest Rohwer 1,2 and Ty N. F. Roach 7 * 1 Department of Biology, San Diego State University, San Diego, CA, United States, 2 Viral Information Institute, San Diego State University, San Diego, CA, United States, 3 Department of Botany, University of British Columbia, Vancouver, BC, Canada, 4 Department of Marine Microbiology and Biogeochemistry, Royal Netherlands Institute for Sea Research (NIOZ), Texel, Netherlands, 5 Department of Geosciences, Faculty of Earth Sciences, Utrecht University, Utrecht, Netherlands, 6 National Center for Biotechnology Information, National Library of Medicine, Bethesda, MD, United States, 7 Hawai‘i Institute of Marine Biology, University of Hawai‘i at M ¯ anoa, K ¯ ane‘ohe, HI, United States, 8 Caribbean Research and Management of Biodiversity (CARMABI), Willemstad, Curaçao, 9 Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands, 10 Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States, 11 Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, San Diego, CA, United States, 12 Department of Biology, University of Miami, Coral Gables, FL, United States, 13 Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, United States All organisms host a diversity of associated viruses, bacteria, and protists, collectively defined as the holobiont. While scientific advancements have enhanced the understanding of the functional roles played by various components of the holobiont, there is a growing need to integrate multiple types of molecular data into spatially and temporally resolved frameworks. To that end, we mapped 16S and 18S rDNA metabarcoding, metatranscriptomics, and metabolomic data onto three-dimensional reconstructions of coral colonies to examine microbial diversity, microbial gene expression, and biochemistry on two colonies of the ecologically important, reef-building coral, Orbicella faveolata and their competitors (i.e., adjacent organisms interacting with the corals: fleshy algae, turf algae, hydrozoans, and other corals). Overall, no statistically significant spatial patterns were observed among the samples for any of the data types; instead, strong signatures of the macroorganismal hosts (e.g., coral, algae, hydrozoa) were detected, in the microbiome, the transcriptome, and the metabolome. The 16S rDNA analysis demonstrated higher abundance of Firmicutes in the coral microbiome than in its competitors. A single bacterial amplicon sequence variant from the genus Clostridium was found exclusively in all O. faveolata samples. In contrast to microbial taxa, a portion of the functionally annotated bacterial RNA transcripts (6.86%) and metabolites (1.95%) were ubiquitous in all coral and competitor samples. Frontiers in Marine Science | www.frontiersin.org 1 April 2021 | Volume 8 | Article 627724