Bacterial Diversity in Replicated Hydrogen Sulfide-Rich Streams
Extreme environments typically require costly adaptations for survival, an attribute that often translates to an elevated influence of habitat conditions on biotic communities. Microbes, primarily bacteria, are successful colonizers of extreme environments worldwide, yet in many instances, the interplay between harsh conditions, dispersal, and microbial biogeography remains unclear. This lack of clarity is particularly true for habitats where extreme temperature is not the overarching stressor, highlighting a need for studies that focus on the role other primary stressors (e.g., toxicants) play in shaping biogeographic patterns. In this study, we leveraged a naturally paired stream system in southern Mexico to explore how elevated hydrogen sulfide (H2S) influences microbial diversity. We sequenced a portion of the 16S rRNA gene using bacterial primers for water sampled from three geographically proximate pairings of streams with high (> 20 μM) or low (~ 0 μM) H2S concentrations. After exploring bacterial diversity within and among sites, we compared our results to a previous study of macroinvertebrates and fish for the same sites. By spanning multiple organismal groups, we were able to illuminate how H2S may differentially affect biodiversity. The presence of elevated H2S had no effect on overall bacterial diversity (p = 0.21), a large effect on community composition (25.8% of variation explained, p < 0.0001), and variable influence depending upon the group—whether fish, macroinvertebrates, or bacteria—being considered. For bacterial diversity, we recovered nine abundant operational taxonomic units (OTUs) that comprised a core H2S-rich stream microbiome in the region. Many H2S-associated OTUs were members of the Epsilonproteobacteria and Gammaproteobacteria, which both have been implicated in endosymbiotic relationships between sulfur-oxidizing bacteria and eukaryotes, suggesting the potential for symbioses that remain to be discovered in these habitats.
Keywords16S sequencing Microbial ecology Toxicity Sulfur oxidation Biogeography Mexico
The authors thank Omar Cornejo for the use of his laboratory space and input, Caren Goldberg for microbial sampling advice, Lisa Orfe for sequencing assistance, Joe Giersch for help producing the sampling map, Lydia Zeglin for statistical input, Anthony Brown and Ryan Greenway for assistance in the field, members of the Kelley and Cornejo labs for manuscript comments, and two anonymous reviewers for their input on the manuscript.
Research was supported by grants from the National Science Foundation (IOS-1557860 to M.T.; IOS-1557795 to J.L.K.), US Army Research Office (W911NF-15-1-0175 to M.T. and J.L.K.), NIH COBRE Phase III (P30GM103324), and the Explorers Club Youth Activity Fund Grant to J.B.P.
- 1.MacArthur RH, Wilson EO (2016) The theory of island biogeography. Princeton university pressGoogle Scholar
- 6.Baas-Becking LGM (1934) Geobiologie; of inleiding tot de milieukunde. WP Van Stockum & Zoon NVGoogle Scholar
- 12.Forte E, Giuffrè A (2016) How bacteria breathe in hydrogen sulfide-rich environments. Biochemist 38:8–11Google Scholar
- 18.Waite DW, Vanwonterghem I, Rinke C, Parks DH, Zhang Y, Takai K, Sievert SM, Simon J, Campbell BJ, Hanson TE (2017) Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.). Frontiers in microbiology 8: 682Google Scholar
- 23.Skirnisdottir S, Hreggvidsson GO, Hjörleifsdottir S, Marteinsson VT, Petursdottir SK, Holst O, Kristjansson JK (2000) Influence of sulfide and temperature on species composition and community structure of hot spring microbial mats. Appl. Environ. Microbiol. 66:2835–2841CrossRefPubMedPubMedCentralGoogle Scholar
- 30.Rosales Lagarde L, Boston P, Campbell A, Stafford K (2006) Possible structural connection between Chichón volcano and the sulfur-rich springs of Villa Luz cave (aka Cueva de las Sardinas), southern Mexico. Assoc Mex Cave Stud Bull 19:177–184Google Scholar
- 34.Gordon A, Hannon G (2010) Fastx-toolkitGoogle Scholar
- 37.Shannon CE, Weaver W (1998) The mathematical theory of communication. University of Illinois pressGoogle Scholar
- 38.Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community Ecol. Packag 10:631–637Google Scholar
- 41.Hamilton N (2015) Ggtern: an extension to ggplot2, for the creation of ternary diagrams. R package version 1Google Scholar
- 45.Inskeep WP, Jay ZJ, Tringe SG, Herrgård MJ, Rusch DB, Committee YMPS, Members WG (2013) The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front. Microbiol. 4Google Scholar
- 48.Padial AA, Ceschin F, Declerck SA, De Meester L, Bonecker CC, Lansac-Tôha FA, Rodrigues L, Rodrigues LC, Train S, Velho LF (2014) Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS One 9:e111227CrossRefPubMedPubMedCentralGoogle Scholar
- 55.Slobodkin A (2014) The family Peptostreptococcaceae. The prokaryotes. Springer, pp. 291–302Google Scholar
- 69.Passow CN, Brown AP, Arias-Rodriquez L, Yee MC, Sockell A, Schartl M, Warren WC, Bustamante C, Kelley JL, Tobler M (2017) Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana, Poeciliidae). Mol. Ecol. 26:4211–4225CrossRefPubMedPubMedCentralGoogle Scholar
- 73.Minic Z, Herve G (2004) Biochemical and enzymological aspects of the symbiosis between the deep-sea tubeworm Riftia pachyptila and its bacterial endosymbiont. FEBS J. 271:3093–3102Google Scholar
- 77.Suzuki Y, Sasaki T, Suzuki M, Nogi Y, Miwa T, Takai K, Nealson KH, Horikoshi K (2005) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. Hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl. Environ. Microbiol. 71:5440–5450CrossRefPubMedPubMedCentralGoogle Scholar