Hydrogenase Gene Distribution and H2 Consumption Ability within the Thiomicrospira Lineage.

Moritz Hansen,Mirjam Perner

doi:10.3389/fmicb.2016.00099

Abstract

Thiomicrospira were originally characterized as sulfur-oxidizing chemolithoautotrophs. Attempts to grow them on hydrogen failed for many years. Only recently we demonstrated hydrogen consumption among two of three tested Thiomicrospira and posited that hydrogen consumption may be more widespread among Thiomicrospira than previously assumed. Here, we investigate and compare the hydrogen consumption ability and the presence of group 1 [NiFe]-hydrogenase genes (enzyme catalyzes H2↔2H+ + 2e-) for sixteen different Thiomicrospira species. Seven of these Thiomicrospira species encoded group 1 [NiFe]-hydrogenase genes and five of these species could also consume hydrogen. All Thiomicrospira species exhibiting hydrogen consumption were from hydrothermal vents along the Mid-Atlantic ridge or Eastern Pacific ridges. The tested Thiomicrospira from Mediterranean and Western Pacific vents could not consume hydrogen. The [NiFe]-hydrogenase genes were categorized into two clusters: those resembling the hydrogenase from Hydrogenovibrio are in cluster I and are related to those from Alpha- and other Gammaproteobacteria. In cluster II, hydrogenases found exclusively in Thiomicrospira crunogena strains are combined and form a monophyletic group with those from Epsilonproteobacteria suggesting they were acquired through horizontal gene transfer. Hydrogen consumption appears to be common among some Thiomicrospira, given that five of the tested sixteen strains carried this trait. The hydrogen consumption ability expands their competitiveness within an environment.

Highlights

Thiomicrospira pelophila was the first Thiomicrospira to be isolated in 1972 from estuarine mud in the Dutch Wadden Sea and was described as a sulfur-oxidizing bacterium (Kuenen and Veldkamp, 1972)
For many years attempts to grow Thiomicrospira species on hydrogen failed (Nishihara et al, 1991; Takai et al, 2004). This was a strain classified as Hydrogenovibrio marinus, which, according to 16S rRNA genes groups with Thiomicrospira, can use hydrogen (Nishihara et al, 1998, 2001). It was not until the genome of T. crunogena XCL-2, isolated from the Galapagos rift vents in the Eastern Pacific (Ahmad et al, 1999), was sequenced and all genes required for a structural [NiFe]-hydrogenase and its assembly and maturation were detected (Scott et al, 2006) that hydrogen oxidation was considered as an alternative energy generation pathway
We found that hydrogen oxidation can be found in different Thiomicrospira strains but that it appears to be limited to few Thiomicrospira lineages

Summary

Consumption Ability within the Thiomicrospira Lineage

Molecular Biology of Microbial Consortia, Biocenter Klein Flottbek, University of Hamburg, Hamburg, Germany. We investigate and compare the hydrogen consumption ability and the presence of group 1 [NiFe]-hydrogenase genes (enzyme catalyzes H2↔2H+ + 2e−) for sixteen different Thiomicrospira species. Seven of these Thiomicrospira species encoded group 1 [NiFe]-hydrogenase genes and five of these species could consume hydrogen. All Thiomicrospira species exhibiting hydrogen consumption were from hydrothermal vents along the Mid-Atlantic ridge or Eastern Pacific ridges. The tested Thiomicrospira from Mediterranean and Western Pacific vents could not consume hydrogen. Hydrogen consumption appears to be common among some Thiomicrospira, given that five of the tested sixteen strains carried this trait.

INTRODUCTION

Metabolism in Thiomicrospira Lineage

MATERIAL AND METHODS

RESULTS AND DISCUSSION

Consumption and Hydrogen Uptake Activity