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Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species.
ISME J. 2019 04; 13(4):902-920.IJ

Abstract

Lucinidae clams harbor gammaproteobacterial thioautotrophic gill endosymbionts that are environmentally acquired. Thioautotrophic lucinid symbionts are related to metabolically similar symbionts associated with diverse marine host taxa and fall into three distinct phylogenetic clades. Most studies on the lucinid-bacteria chemosymbiosis have been done with seagrass-dwelling hosts, whose symbionts belong to the largest phylogenetic clade. In this study, we examined the taxonomy and functional repertoire of bacterial endosymbionts at an unprecedented resolution from Phacoides pectinatus retrieved from mangrove-lined coastal sediments, which are underrepresented in chemosymbiosis studies. The P. pectinatus thioautotrophic endosymbiont expressed metabolic gene variants for thioautotrophy, respiration, and nitrogen assimilation distinct from previously characterized lucinid thioautotrophic symbionts and other marine symbionts. At least two other bacterial species with different metabolisms were also consistently identified in the P. pectinatus gill microbiome, including a Kistimonas-like species and a Spirochaeta-like species. Bacterial transcripts involved in adhesion, growth, and virulence and mixotrophy were highly expressed, as were host-related hemoglobin and lysozyme transcripts indicative of sulfide/oxygen/CO2 transport and bactericidal activity. This study suggests the potential roles of P. pectinatus and its gill microbiome species in mangrove sediment biogeochemistry and offers insights into host and microbe metabolisms in the habitat.

Authors+Show Affiliations

Department of Biological Sciences, Clemson University, Clemson, SC, 29634-0001, USA.Department of Biological Sciences, Clemson University, Clemson, SC, 29634-0001, USA. College of Medicine, Medical University of South Carolina, Charleston, SC, 29425-8900, USA.Department of Biological Sciences, Clemson University, Clemson, SC, 29634-0001, USA. Instituto de Medicina Tropical São Paulo, Universidade de São Paulo, São Paulo, 05403-000, Brazil.Department of Biological Sciences, Clemson University, Clemson, SC, 29634-0001, USA.Department of Biological Sciences, Clemson University, Clemson, SC, 29634-0001, USA.Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, TN, 37996-1410, USA.Department of Geology and Geological Engineering, South Dakota School of Mines and Technology, Rapid City, SD, 57701-3901, USA.Department of Biological Sciences, Clemson University, Clemson, SC, 29634-0001, USA. bcampb7@clemson.edu.

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

30518817

Citation

Lim, Shen Jean, et al. "Taxonomic and Functional Heterogeneity of the Gill Microbiome in a Symbiotic Coastal Mangrove Lucinid Species." The ISME Journal, vol. 13, no. 4, 2019, pp. 902-920.
Lim SJ, Davis BG, Gill DE, et al. Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species. ISME J. 2019;13(4):902-920.
Lim, S. J., Davis, B. G., Gill, D. E., Walton, J., Nachman, E., Engel, A. S., Anderson, L. C., & Campbell, B. J. (2019). Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species. The ISME Journal, 13(4), 902-920. https://doi.org/10.1038/s41396-018-0318-3
Lim SJ, et al. Taxonomic and Functional Heterogeneity of the Gill Microbiome in a Symbiotic Coastal Mangrove Lucinid Species. ISME J. 2019;13(4):902-920. PubMed PMID: 30518817.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species. AU - Lim,Shen Jean, AU - Davis,Brenton G, AU - Gill,Danielle E, AU - Walton,Jillian, AU - Nachman,Erika, AU - Engel,Annette Summers, AU - Anderson,Laurie C, AU - Campbell,Barbara J, Y1 - 2018/12/05/ PY - 2018/04/26/received PY - 2018/11/04/accepted PY - 2018/10/23/revised PY - 2018/12/7/pubmed PY - 2019/8/20/medline PY - 2018/12/7/entrez SP - 902 EP - 920 JF - The ISME journal JO - ISME J VL - 13 IS - 4 N2 - Lucinidae clams harbor gammaproteobacterial thioautotrophic gill endosymbionts that are environmentally acquired. Thioautotrophic lucinid symbionts are related to metabolically similar symbionts associated with diverse marine host taxa and fall into three distinct phylogenetic clades. Most studies on the lucinid-bacteria chemosymbiosis have been done with seagrass-dwelling hosts, whose symbionts belong to the largest phylogenetic clade. In this study, we examined the taxonomy and functional repertoire of bacterial endosymbionts at an unprecedented resolution from Phacoides pectinatus retrieved from mangrove-lined coastal sediments, which are underrepresented in chemosymbiosis studies. The P. pectinatus thioautotrophic endosymbiont expressed metabolic gene variants for thioautotrophy, respiration, and nitrogen assimilation distinct from previously characterized lucinid thioautotrophic symbionts and other marine symbionts. At least two other bacterial species with different metabolisms were also consistently identified in the P. pectinatus gill microbiome, including a Kistimonas-like species and a Spirochaeta-like species. Bacterial transcripts involved in adhesion, growth, and virulence and mixotrophy were highly expressed, as were host-related hemoglobin and lysozyme transcripts indicative of sulfide/oxygen/CO2 transport and bactericidal activity. This study suggests the potential roles of P. pectinatus and its gill microbiome species in mangrove sediment biogeochemistry and offers insights into host and microbe metabolisms in the habitat. SN - 1751-7370 UR - https://www.unboundmedicine.com/medline/citation/30518817/Taxonomic_and_functional_heterogeneity_of_the_gill_microbiome_in_a_symbiotic_coastal_mangrove_lucinid_species L2 - http://dx.doi.org/10.1038/s41396-018-0318-3 DB - PRIME DP - Unbound Medicine ER -