Organohalide-Respiring Bacteria at the Heart of Anaerobic Metabolism in Arctic Wet Tundra Soils

Abstract

Recent work revealed an active biological chlorine cycle in coastal Arctic tundra of northern Alaska. This raised the question of whether chlorine cycling was restricted to coastal areas or if these processes extended to inland tundra. The anaerobic process of organohalide respiration, carried out by specialized bacteria like Dehalococcoides, consumes hydrogen gas and acetate using halogenated organic compounds as terminal electron acceptors, potentially competing with methanogens that produce the greenhouse gas methane. We measured microbial community composition and soil chemistry along an ∼262-km coastal-inland transect to test for the potential of organohalide respiration across the Arctic Coastal Plain and studied the microbial community associated with Dehalococcoides to explore the ecology of this group and its potential to impact C cycling in the Arctic. Concentrations of brominated organic compounds declined sharply with distance from the coast, but the decrease in organic chlorine pools was more subtle. The relative abundances of Dehalococcoides were similar across the transect, except for being lower at the most inland site. Dehalococcoides correlated with other strictly anaerobic genera, plus some facultative ones, that had the genetic potential to provide essential resources (hydrogen, acetate, corrinoids, or organic chlorine). This community included iron reducers, sulfate reducers, syntrophic bacteria, acetogens, and methanogens, some of which might also compete with Dehalococcoides for hydrogen and acetate. Throughout the Arctic Coastal Plain, Dehalococcoides is associated with the dominant anaerobes that control fluxes of hydrogen, acetate, methane, and carbon dioxide. Depending on seasonal electron acceptor availability, organohalide-respiring bacteria could impact carbon cycling in Arctic wet tundra soils.IMPORTANCE Once considered relevant only in contaminated sites, it is now recognized that biological chlorine cycling is widespread in natural environments. However, linkages between chlorine cycling and other ecosystem processes are not well established. Species in the genus Dehalococcoides are highly specialized, using hydrogen, acetate, vitamin B₁₂-like compounds, and organic chlorine produced by the surrounding community. We studied which neighbors might produce these essential resources for Dehalococcoides species. We found that Dehalococcoides species are ubiquitous across the Arctic Coastal Plain and are closely associated with a network of microbes that produce or consume hydrogen or acetate, including the most abundant anaerobic bacteria and methanogenic archaea. We also found organic chlorine and microbes that can produce these compounds throughout the study area. Therefore, Dehalococcoides could control the balance between carbon dioxide and methane (a more potent greenhouse gas) when suitable organic chlorine compounds are available to drive hydrogen and acetate uptake.

Keywords: Arctic; Dehalococcoides; chlorine; methanogenesis; soil.

FIG 1

Chloride concentrations in precipitation at sites along a coastal-inland transect starting near the Beaufort Sea.

FIG 2

Total and organic halogens (bromine [A] and chlorine [B]) in soils from the eight study locations, arranged from most coastal on the left to furthest inland on the right. In regressions on the log-transformed distance from the coast, Br_org declined significantly (P = 0.004), while Cl_org did not (P = 0.195).

FIG 3

Acid-extractable Fe (A) and soluble e⁻ acceptors (B) from sites along the coastal-inland transect, integrated over a 35-cm soil profile. The nitrate concentrations and ratios of Fe(III)/total Fe were significantly higher at IVO and TFS (P = 0.001).

FIG 4

Concentrations of formate (A) and acetate (B) in soils by depth and location along the coastal-inland transect. Soil concentrations of acetate (P = 0.008) and formate (P = 0.001) differed significantly by site, while the concentration of formate was also significantly higher (P = 0.006) in deeper soil layers.

FIG 5

Nonmetric multidimensional scaling (NMDS) analysis of 64 soil metagenomes showing samples by depth (symbols) and location (color). Data in panels A to C are based on taxonomic data (at the phylum level except for Proteobacteria, which were separated by class [stress = 0.092]), and data in panel D are based on functional data (SEED subsystem level 2 [stress = 0.17]). The 95% confidence ellipses around the centroids for each group are drawn for location (A and D) and depth (B). Taxonomically, IVO is significantly different from the other sites, and all 3 depths are different from each other. Functionally, all sites and depths differ significantly. Significant environmental variables are overlaid on taxonomic (C) and functional gene (D) ordinations. Ca, Cl, Fe, Fe(II), formate, NO₃, and SO₄ represent concentrations of these chemical species on a soil volume basis, while wFe and aFe are the ratios of Fe(II) to total Fe for water- and acid-extractable pools, respectively.

FIG 6

Relative abundance (percent) of indicator taxa for anaerobic processes by depth and location along the transect. The effects of site were significant for all indicator taxa (P < 0.001), and depth was significant for all indicators (P < 0.05) except Geobacter (P = 0.233). SRB, sulfate-reducing bacteria.

FIG 7

Network of genera associated with Dehalococcoides and their potential to provide essential resources. Genera are arranged axially according to their correlation (R) with Dehalococcoides, with stronger correlations grouped toward the center, and radially according to phyla (note that Caldithrix is the sole representative of its phylum). Colored lines indicate the genetic potential of each to provide an essential resource to Dehalococcoides. See the text regarding possible Cl_org synthesis by Salinibacter. Genera below ∼0.1% abundance are not shown. COD, carbon monoxide dehydrogenase; ACS, acetyl CoA synthase; AcK, acetate kinase.

FIG 8

Potential interactions among the functional groups shown in Fig. 7 with respect to H₂ and acetate cycling and the production of CO₂ and CH₄. Double-sided arrows for Fe and sulfate reducers show that H₂ can be produced or consumed, depending on the availability of terminal e⁻ acceptors (shown in blue).