Taphonomy of microorganisms and microbial microtextures at sulfidic hydrothermal vents: A case study from the Roman Ruins black smokers, Eastern Manus Basin

Abstract

Biological activity at deep‐sea hydrothermal chimneys is driven by chemotrophic microorganisms that metabolize chemicals from the venting high‐temperature fluids. Understanding taphonomy and microbial microtextures in such environments is a necessity for micropaleontological and palaeoecological research. This study examines fossilized microorganisms and related microtextures in a recent black smoker from the Roman Ruins hydrothermal vent site, Eastern Manus Basin offshore of Papua New Guinea. Whereas the center of the examined sulfide chimney is dominated by high‐temperature mineralogy (chalcopyrite and dendritic sphalerite), filamentous and coccoidal biomorphs occur in an outer, warm zone of mixing between hydrothermal fluids and seawater, which is indicated by their occurrence within colloform and botryoidal pyrite of barite–pyrite coprecipitates. Both morphotypes can be interpreted as thermophilic microorganisms based on their occurrence in a high‐temperature habitat. Their separate (non‐commensal) occurrence hints at sensitivities to microenvironmental conditions, which is expectable for strong temperature, pH, and redox gradients at the walls of deep‐sea hydrothermal chimneys. Whereas both morphotypes experienced mild thermal overprint, taphonomic differences exist: (i) spaces left by cells in filamentous fossils are predominately filled by silica, whereas inter/extracellular features (crosswalls/septae and outer sheaths) are pyritized; (ii) coccoidal fossils show both silica‐ and pyrite‐infilled interiors, and generally better preservation of cell walls. These different manifestations presumably relate to an interplay between microenvironmental and biological factors, potentially contrasting metabolisms, and differences in cell wall chemistries of distinct bacteria and/or archaea. A further hypothesis is that the coccoidal features represent biofilm‐forming organisms, whose organic matter derivates contributed to the formation of intimately associated wavy and wrinkly carbonaceous laminations that are at least locally distinguishable from the texture of the surrounding pyrite. Hence, the presented data provide evidence that microtextures of microbiota from hydrothermal systems can have a similar significance for palaeobiological research as those from sedimentary environments.

Microbial biosignatures in ancient deep‐sea hydrothermal sulfides

“…Moreover, the organic compounds contributing to this auto‐assembly may derive from the degradation of primary organic matter that does not testify to a biogenic origin of associated minerals (Brasier et al, 2002; Simoneit, 1993; Simoneit et al, 2004). Pyritization of such abiotic filaments may yield features resembling previously reported pyritized microfossils in hydrothermal sulfides (Baumgartner et al, 2022; Rasmussen, 2000). The morphological preservation of abiotic biomorphs needs to be tested for hydrothermal conditions, but likely, such features can easily be confused with microbial microfossils in ancient rocks.…”

“…Pyritization of such abiotic filaments may yield features resembling previously reported pyritized microfossils in hydrothermal sulfides (Baumgartner et al, 2022;Rasmussen, 2000). The morphological preservation of abiotic biomorphs needs to be tested for hydrothermal conditions, but likely, such features can easily be confused with microbial microfossils in ancient rocks.…”

“…Biofilms, microbial mats as well as microbialite‐like rock fabrics formed by benthic microbial communities are present in today's deep‐sea hydrothermal systems (Baumgartner et al, 2022; Blumenberg et al, 2007; Flemming & Wuertz, 2019; Moeller et al, 2014; Reysenbach & Cady, 2001; Van Dover, 2000, 2019). Moreover, numerous Fe sulfide‐bearing microbialites in the Precambrian hydrothermal deposits demonstrate their preservation potential over billion‐year timescales (Baumgartner et al, 2019; Baumgartner, Caruso, et al, 2020; Baumgartner, Van Kranendonk, et al, 2020; Duda et al, 2016; McGoldrick, 1999; Mißbach et al, 2021; Van Kranendonk et al, 2008; Figure 1a).…”

“…It may be fostered by biologically induced precipitation and/or encrustation of organic templates of biofilms and microbial mats in Fe and S minerals (see the section on Mineral precipitates). These structures may serve as precursors for the secondary sulfidation of Fe minerals and organic matter driven by reduced sulfur species from volcanic exhalation or microbial sulfur cycling (Baumgartner et al, 2022; Campbell, 2006; Kelley et al, 2002; Little et al, 1998; Russell, 1996). The fabric, texture, and mineralogy of microbialites in deep‐sea hydrothermal systems will likely depend on temperature, pH, and fluid chemistry.…”

Prokaryotic community structure and key taxa in the Arabian Sea’s oxygen minimum zone

“…The oceans boast a captivating ecosystem, replete with diverse habitats like cold seeps, hydrothermal vents, and oxygen minimum zones (OMZs) (Li et al, 2021b;Baumgartner et al, 2022;Chen et al, 2022). The microbial community inhabiting each habitat play a pivotal role in governing the oceans' biogeochemical cycles, actively engaging in nearly all oceanic biogeochemical processes.…”