Comparative Analysis of Microbial Communities in Iron-Dominated Flocculent Mats in Deep-Sea Hydrothermal Environments

Abstract

It has been suggested that iron is one of the most important energy sources for photosynthesis-independent microbial ecosystems in the ocean crust. Iron-metabolizing chemolithoautotrophs play a key role as primary producers, but little is known about their distribution and diversity and their ecological role as submarine iron-metabolizing chemolithotrophs, particularly the iron oxidizers. In this study, we investigated the microbial communities in several iron-dominated flocculent mats found in deep-sea hydrothermal fields in the Mariana Volcanic Arc and Trough and the Okinawa Trough by culture-independent molecular techniques and X-ray mineralogical analyses. The abundance and composition of the 16S rRNA gene phylotypes demonstrated the ubiquity of zetaproteobacterial phylotypes in iron-dominated mat communities affected by hydrothermal fluid input. Electron microscopy with energy-dispersive X-ray microanalysis and X-ray absorption fine structure (XAFS) analysis revealed the chemical and mineralogical signatures of biogenic Fe-(oxy)hydroxide species and the potential contribution of Zetaproteobacteria to the in situ generation. These results suggest that putative iron-oxidizing chemolithoautotrophs play a significant ecological role in producing iron-dominated flocculent mats and that they are important for iron and carbon cycles in deep-sea low-temperature hydrothermal environments. IMPORTANCEWe report novel aspects of microbiology from iron-dominated flocculent mats in various deep-sea environments. In this study, we examined the relationship between Zetaproteobacteria and iron oxides across several hydrothermally influenced sites in the deep sea. We analyzed iron-dominated mats using culture-independent molecular techniques and X-ray mineralogical analyses. The scanning electron microscopy-energy-dispersive X-ray spectroscopy SEM-EDS analysis and X-ray absorption fine structure (XAFS) analysis revealed chemical and mineralogical signatures of biogenic Fe-(oxy)hydroxide species as well as the potential contribution of the zetaproteobacterial population to the in situ production. These key findings provide important information for understanding the mechanisms of both geomicrobiological iron cycling and the formation of iron-dominated mats in deepsea hydrothermal fields. Iron is one of the most common elements on Earth and is the fourth most abundant element in the Earth's crust. Iron has a wide range of oxidation states but exists mostly in a ϩ2 or ϩ3 state in the natural environment. The valence of iron depends on the prevailing environmental physicochemical conditions, such as pH, O 2 concentration, and redox potential. Iron occurs in many mineral phases, including (hydr)oxides, carbonates, silicates, and sulfides. The oxidation of ferrous to ferric iron releases energy, which is harnessed by some iron-oxidizing prokaryotes. Ferrous iron is stable under anoxic conditions but can autoxidize in air. Some microbial communities that are unable to use solar energy via photosynthesis use energy from iron ...

Community Structure of Lithotrophically-Driven Hydrothermal Microbial Mats from the Mariana Arc and Back-Arc

“…The two other groups are composed of communities from Snail, Urashima, and NW Rota-1, which are all relatively close to one another whereas NW Eifuku is hundreds of km north of these three vent fields (Figure 1A ). These data support previous research showing community structure variability corresponding with vent location (Opatkiewicz et al, 2009 ; Huber et al, 2010 ; Makita et al, 2016 ). Although there were OTUs with significantly different abundances among all three groups of iron-dominated mats as determined via Metastats (Figure 3 ), there were no genera unique to one grouping, which suggests that a common ecosystem function is shared among the abundant community members of the Zeta-, Epsilon-, and Gamma-proteobacterial OTUs in all iron-dominated mats of the Mariana Arc and back-arc.…”

“…All characterized Zetaproteobacteria strains are obligate iron-oxidizing lithoautotrophs belonging to the genus Mariprofundus (Emerson et al, 2007 ; McBeth et al, 2011 ; Makita et al, 2017 ). Members of this genus have been previously detected in flocculent mats from the back-arc Snail and Urashima sites and from NW Eifuku (Davis and Moyer, 2008 ; Kato et al, 2009a ; Makita et al, 2016 ); in addition to these locations, we have now identified Zetaproteobacteria at NW Rota-1 (Olde Iron Slides). After years of documented eruptions from 2004 to 2010 (Schnur et al, 2017 ), it is possible the hydrothermal fluids are undergoing a transition from sulfur- to iron-dominated effluent at this location as hypothesized by Butterfield et al ( 1997 ).…”

“…This increased biodiversity is potentially due to the Fe-oxyhydroxides produced by the Zetaproteobacteria. These extracellular structures (e.g., stalks and sheaths) are well-documented from both isolates and naturally occurring microbial mats (Fleming et al, 2013 ; Bennett et al, 2014 ; Chan et al, 2016b ; Makita et al, 2016 ). This high surface-area architecture can be colonized by an array of secondary consumers (e.g., Bacteroidetes, Chloroflexi, Gammaproteobacteria, and Planctomycetes) that were also found to be present (Figure 2 ).…”

Validating the Cyc2 Neutrophilic Iron Oxidation Pathway Using Meta-omics of Zetaproteobacteria Iron Mats at Marine Hydrothermal Vents

“…To this end, we turned to Zetaproteobacteria in natural Fe microbial mats. The Zetaproteobacteria discovered to date are all considered to be Fe oxidizers, since every isolate grows by Fe oxidation and uncultured Zetaproteobacteria are typically found in Fe-oxidizing environments (10,(16)(17)(18)(19)(20)(21). The Zetaproteobacteria are often the dominant organisms in marine hydrothermal Fe mats (22)(23)(24)(25), where they play a key role in mat formation (26).…”

Effects of Organic Amendments on the Transformation of Fe (Oxyhydr)Oxides and Soil Organic Carbon Storage

“…A variety of Fe (oxyhydr)oxide forms and crystallinities coexist in soils and can be transformed to one another as a result of Fe redox cycling driven by both abiotic and biotic processes (Fortin and Langley, 2005;Kappler and Straub, 2005). The biotic transformations of Fe (oxyhydr)oxides mediated by microorganisms in most soils and sediments are often much faster than the corresponding abiotic reactions (Weber et al, 2006a).…”