Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities - PubMed (original) (raw)

Microbial diversity of hydrothermal sediments in the Guaymas Basin: evidence for anaerobic methanotrophic communities

Andreas Teske et al. Appl Environ Microbiol. 2002 Apr.

Abstract

Microbial communities in hydrothermally active sediments of the Guaymas Basin (Gulf of California, Mexico) were studied by using 16S rRNA sequencing and carbon isotopic analysis of archaeal and bacterial lipids. The Guaymas sediments harbored uncultured euryarchaeota of two distinct phylogenetic lineages within the anaerobic methane oxidation 1 (ANME-1) group, ANME-1a and ANME-1b, and of the ANME-2c lineage within the Methanosarcinales, both previously assigned to the methanotrophic archaea. The archaeal lipids in the Guaymas Basin sediments included archaeol, diagnostic for nonthermophilic euryarchaeota, and sn-2-hydroxyarchaeol, with the latter compound being particularly abundant in cultured members of the Methanosarcinales. The concentrations of these compounds were among the highest observed so far in studies of methane seep environments. The delta-(13)C values of these lipids (delta-(13)C = -89 to -58 per thousand) indicate an origin from anaerobic methanotrophic archaea. This molecular-isotopic signature was found not only in samples that yielded predominantly ANME-2 clones but also in samples that yielded exclusively ANME-1 clones. ANME-1 archaea therefore remain strong candidates for mediation of the anaerobic oxidation of methane. Based on 16S rRNA data, the Guaymas sediments harbor phylogenetically diverse bacterial populations, which show considerable overlap with bacterial populations of geothermal habitats and natural or anthropogenic hydrocarbon-rich sites. Consistent with earlier observations, our combined evidence from bacterial phylogeny and molecular-isotopic data indicates an important role of some novel deeply branching bacteria in anaerobic methanotrophy. Anaerobic methane oxidation likely represents a significant and widely occurring process in the trophic ecology of methane-rich hydrothermal vents. This study stresses a high diversity among communities capable of anaerobic oxidation of methane.

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Figures

FIG. 1.

FIG. 1.

Reconstructed ion chromatogram of alcohol fraction from core A sample, 0 to 1 cm. Colors of peaks designate their biological sources: red, methanotrophic archaea; blue, presumed bacterial members of methanotrophic community; orange, aerobic bacteria; green, eucaryotes, e.g., marine algae. Refer to Table 1 for further details.

FIG. 2.

FIG. 2.

Distance tree of archaeal clones from Guaymas sediment cores A, C, and T, based on near-complete 16S rDNA sequences. Bootstrap values (in percent) are based on 1,000 replicates each (distance and parsimony) and are shown for branches with more than 50% bootstrap support. The sequence for Methanohalophilus zhilinae was obtained from the ARB sequence server (version May 2001). Crenarchaeotal sequences SB-pc17-1A10 and Eel-36a2H12 were provided by Victoria Orphan. For the major phylogenetic divisions, the numbers of core A, core C, and core T clones are given in that order. For multiple near-identical clones (>99% identity), the number of multiples is given after the GenBank number of a representative clone. Some sequence types occurred in several sediment layers: Guaymas clone A1 R010 was found four times in the 0- to 1-cm layer of core A and two times in the 1- to 2-cm layer of core A. Guaymas clone A2 R045 was found 15 times in the 0- to 1-cm layer of core A and 2 times in the 1- to 2-cm layer of core A. Guaymas clone T R022 was found one time in the 0- to 1-cm layer of core C and one time in core T.

FIG. 3.

FIG. 3.

Distance tree of proteobacterial clones from Guaymas sediment cores A and C, based on near-complete 16S rDNA sequences. Bootstrap values (in percent) are based on 1,000 replicates each (distance and parsimony) and are shown for branches with more than 50% bootstrap support. For the major phylogenetic divisions, the numbers of core A and core C clones are given in that order. For multiple near-identical clones (>99% identity), the number of multiples is given after the GenBank number of a representative clone. Some sequence types occurred in several sediment layers: Guaymas clone A1 B030 was found three times in the 0- to 1-cm layer of core A and one time in the 1- to 2-cm layer of core A, Guaymas clone A2 B043 was found one time in the 0- to 1-cm layer of core A and five times in the 1- to 2-cm layer of core A, and Guaymas clone A2 B004 was found three times in the 0- to 1-cm layer of core A and three times in the 1- to 2-cm layer of core A.

FIG. 4.

FIG. 4.

Distance tree of bacterial clones, excluding proteobacteria, from Guaymas sediment cores A and C, based on near-complete 16S rDNA sequences. Bootstrap values (in percent) are based on 1,000 replicates each (distance and parsimony) and are shown for branches with more than 50% bootstrap support. For the major phylogenetic divisions, the numbers of core A and core C clones are given in that order. For multiple near-identical clones (>99% identity), the number of multiples is given after the GenBank number of a representative clone. Some sequence types occurred in several sediment layers: Guaymas clone A1 B007 was found two times in the 0- to 1-cm layer and one time in the 1- to 2-cm layer of core A, Guaymas clone A2 B031 was found two times in the 0- to 1-cm layer and one time in the 1- to 2-cm layer of core A, Guaymas clone A1 B020 was found three times in the 0- to 1-cm layer and two times in the 1- to 2-cm layer of core A, and Guaymas clone A2 B002 was found one time in the 0- to 1-cm layer and two times in the 1- to 2-cm layer of core A.

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