Lava cave microbial communities within mats and secondary mineral deposits: implications for life detection on other planets

Abstract

Lava caves contain a wealth of yellow, white, pink, tan, and gold-colored microbial mats; but in addition to these clearly biological mats, there are many secondary mineral deposits that are nonbiological in appearance. Secondary mineral deposits examined include an amorphous copper-silicate deposit (Hawai'i) that is blue-green in color and contains reticulated and fuzzy filament morphologies. In the Azores, lava tubes contain iron-oxide formations, a soft ooze-like coating, and pink hexagons on basaltic glass, while gold-colored deposits are found in lava caves in New Mexico and Hawai'i. A combination of scanning electron microscopy (SEM) and molecular techniques was used to analyze these communities. Molecular analyses of the microbial mats and secondary mineral deposits revealed a community that contains 14 phyla of bacteria across three locations: the Azores, New Mexico, and Hawai'i. Similarities exist between bacterial phyla found in microbial mats and secondary minerals, but marked differences also occur, such as the lack of Actinobacteria in two-thirds of the secondary mineral deposits. The discovery that such deposits contain abundant life can help guide our detection of life on extraterrestrial bodies.

FIG. 1.

Photos illustrate an opening to a lava cave in a volcanic trench (A), the entrance to Four Windows Cave from the inside of the cave (B), a skylight in Four Windows Cave (C), a typical lava cave shape in El Malpais (D). All photos are from El Malpais National Monument and are copyright Kenneth Ingham; used with permission. Color images available online at www.liebertonline.com/ast

FIG. 2.

Microbial mats from Azorean lava caves. (A) Yellow microbial mats coat the lava cave wall. (B) White and pinkish-tan microbial colonies from a lava cave wall. (C) White and tan colonies on a wall that is dripping water. (D) White and tan microbial colonies adorn a lavacicle on the cave ceiling. (E) Yellow and white microbial mats from a lava cave wall. Field of view is approximately 2.5 m (A), 5 cm (B), 6 cm (C), 2 cm (D), and 4 cm (E) across. Images courtesy of Kenneth Ingham; used with permission. Color images available online at www.liebertonline.com/ast

FIG. 3.

Blue-green, copper-containing deposits from the Maelstrom entrance of the Kipuka Kanohina Cave Preserve, Hawai‘i. Width of drip≈0.5 cm. Image courtesy of Kenneth Ingham; used with permission. Color images available online at www.liebertonline.com/ast

FIG. 4.

Pointillistic features from the wall of Epperson's Cave. (A) Two-centimeter overview of macroscopic deposits. Image courtesy of Kenneth Ingham; used with permission. (B) Overview of iron-oxide biofilm with unerupted colonies. (C) Scanning electron micrograph close-up view of the iron-oxide (FeOX) biofilm with colonies that are getting ready to erupt. (D) Newly erupted colony.

FIG. 5.

Iron-oxide formations in Gruta dos Buracos in the Azores. Image courtesy of Kenneth Ingham; used with permission. Color images available online at www.liebertonline.com/ast

FIG. 6.

Butterscotch-colored ooze forming a filigree in Gruta dos Principiantes in the Azores. Color images available online at www.liebertonline.com/ast

FIG. 7.

Pink hexagons on basaltic glass in Algar do Carvão, the Azores. (A) Overview of the pink hexagons; (B) close-up view from (A). Color images available online at www.liebertonline.com/ast

FIG. 8.

Gold-colored secondary minerals on the walls and in cracks of Four Windows Cave in El Malpais National Monument, New Mexico (A, B) and in Thurston Lava Tube, in Hawai‘i Volcanoes National Park (C). Images courtesy of Kenneth Ingham; used with permission. Color images available online at www.liebertonline.com/ast

FIG. 9.

Comparison of the phyla present in the secondary mineral deposits. TH12-G=gold-colored deposits in Thurston Lava Tube, Hawai‘i; 4W7-G=Gold deposits in Four Windows Cave, New Mexico; AC30-PH=Pink hexagons in Algar do Carvão, Azores; GB24-10=Iron-oxide formation in Gruta dos Buracos; GP27-8 BS=Butterscotch filigree in Gruta dos Principiantes, the Azores; MA4-BG=Blue-green deposits in the Maelstrom section of Kipuka Kanohina Cave Preserve, Hawai‘i; KAU-Y=Kaumana Cave, Hawai‘i.

FIG. 10.

Scanning electron microscope images of microbial mats showing a variety of biological morphologies. (A) Filaments with extensive putative pili covering their surfaces, (B) coccoid forms with pili or filamentous extracellular polymeric substances, and (C) beads-on-a-string and rods arranged in rows.

FIG. 11.

Details of the blue-green deposits. (A) Overview of reticulated filaments overlying Actinobacteria-like morphologies. (B) Closer view showing reticulated morphology from one of the clusters of filamentous forms in (A) (Melim et al., 2008). (C) EDX of blue-green deposit showing Si, O, Cu, Al. Traces of Ca and Mg are also present. (D) X-ray diffraction pattern of blue-green deposit compared to pattern for chrysocolla; pattern indicates the blue-green deposit is amorphous chrysocolla. Color images available online at www.liebertonline.com/ast

FIG. 12.

Scanning electron microscope images of gold-colored vein deposits. (Left) Filaments and fuzzy coccoid/filament morphologies from Thurston Lava Tube, Hawai‘i. (Right) Filamentous morphologies from Four Windows Cave, New Mexico.

FIG. 13.

Scanning electron microscope images of pink hexagons. (A) Overview of a field of pink hexagons. (B) Closer view of one of the hexagons that shows some degradation of the hexagon. (C) Close-up view of detail from (B), showing the coated filaments inhabiting the upper surface of the hexagon. (D) EDX analysis of the hexagons showing the presence of iron oxides and a possible opal coating (Si, O). (E) Close-up view of the coated filaments that inhabit the surfaces of hexagons. (F) Small- and large-diameter filaments have colonized the basaltic glass between hexagons. Color images available online at www.liebertonline.com/ast