Characterization of Chemosynthetic Microbial Mats Associated with Intertidal Hydrothermal Sulfur Vents in White Point, San Pedro, CA, USA

Abstract

The shallow-sea hydrothermal vents at White Point (WP) in Palos Verdes on the southern California coast support microbial mats and provide easily accessed settings in which to study chemolithoautotrophic sulfur cycling. Previous studies have cultured sulfur-oxidizing bacteria from the WP mats; however, almost nothing is known about the in situ diversity and activity of the microorganisms in these habitats. We studied the diversity, micron-scale spatial associations and metabolic activity of the mat community via sequence analysis of 16S rRNA and aprA genes, fluorescence in situ hybridization (FISH) microscopy and sulfate reduction rate (SRR) measurements. Sequence analysis revealed a diverse group of bacteria, dominated by sulfur cycling gamma-, epsilon-, and deltaproteobacterial lineages such as Marithrix, Sulfurovum, and Desulfuromusa. FISH microscopy suggests a close physical association between sulfur-oxidizing and sulfur-reducing genotypes, while radiotracer studies showed low, but detectable, SRR. Comparative 16S rRNA gene sequence analyses indicate the WP sulfur vent microbial mat community is similar, but distinct from other hydrothermal vent communities representing a range of biotopes and lithologic settings. These findings suggest a complete biological sulfur cycle is operating in the WP mat ecosystem mediated by diverse bacterial lineages, with some similarity with deep-sea hydrothermal vent communities.

Ecological Succession of Sulfur-Oxidizing Epsilon- and Gammaproteobacteria During Colonization of a Shallow-Water Gas Vent

“…Sequences related to the genus B46 within Gammaproteobacteria with 95% similarity to Methylomolas and Methylococcaceae were also recovered. Similar sequences have been recovered from the Tica vent on the East Pacific Rise deep-sea hydrothermal vent system (GenBank accession number KT257824) (Gulmann et al, 2015) as well as microbial mats at White Point, California (GenBank accession number KX422153) (Miranda et al, 2016) indicating potential occurrence of methylotrophy in addition to chemoautotrophy. Successful isolation of Sedimenticola thiotaurini , another sulfur-oxidizing chemolithotroph belonging to Gammaproteobacteria , further confirmed their dominance in the EF.…”

“…Previous field observations of the distribution of microorganisms in biofilms from geothermal habitats indicated that Epsilon - and Gammaproteobacteria are spatially segregated, with the former dominating higher sulfide habitats and the latter being more prevalent in lower sulfide, possibly more oxic habitats (Engel et al, 2004; Reigstad et al, 2011; Giovannelli et al, 2013; O’Brien et al, 2015; Miranda et al, 2016). Based on these observations, and on the high concentrations of sulfide measured in the gases at Tor Caldara (Table 1), we had predicted that the EF biofilms would be dominated by sulfide-oxidizing Epsilonproteobacteria .…”

“…Microbial biofilms have been studied at cold seeps (Ristova et al, 2015; Paul et al, 2017), sulfidic caves (Engel et al, 2004; Macalady et al, 2006), thermal springs (Coman et al, 2013; Beam et al, 2016), mud volcanoes (Heijs et al (2005); Omoregie et al, 2008), as well as deep-sea (Lopez-Garcia et al, 2003; Alain et al, 2004; Crépeau et al, 2011; Dahle et al, 2013; Gulmann et al, 2015; O’Brien et al, 2015; Stokke et al, 2015; Teske et al, 2016) and shallow-water vents (Gugliandolo et al, 2006; Miranda et al, 2016). Many of these microbial communities are dominated by members of the Gammaproteobacteria and Epsilonproteobacteria (Macalady et al, 2006; Crépeau et al, 2011; O’Brien et al, 2015).…”

“…Sequences related to the genus Sulfurospirillum were also recovered. Both genera are sulfur-oxidizing chemolithoautotrophic members of Epsilonproteobacteria that are abundant in both shallow and deep-sea vents environments (Sievert and Vetriani, 2012; Giovannelli et al, 2013; Vetriani et al, 2014; O’Brien et al, 2015; Miranda et al, 2016). We also isolated a pure culture from Tor Caldara that had ∼93% 16S rRNA gene sequence similarity to Sulfurimonas gotlandica , which is another sulfur-oxidizing chemolithoautotrophic Epsilonproteobacterium .…”

Bacterial Diversity and Biogeochemistry of Two Marine Shallow-Water Hydrothermal Systems off Dominica (Lesser Antilles)

“…Therefore, in addition to chemosynthetic processes, microbial communities of shallow-water systems may also use light for the production of biomass via photosynthesis, resulting in high biological productivity and likely even more complex microbial communities relative to the deep-sea counterparts (Wang et al, 2015 ). Despite this, little is known about the ecology of microbial communities of shallow-water hydrothermal systems and they remain largely understudied compared to their deep-sea counterparts (Dawson et al, 2016 ; Miranda et al, 2016 ; Gomez-Saez et al, 2017 ).…”