Methane- and dissolved organic carbon-fueled microbial loop supports a tropical subterranean estuary ecosystem

D Brankovits,M B Leigh,M F Lehmann,F Alvarez,T M Iliffe,B Phillips,M C Leewis,K W Becker,J W Pohlman,H Niemann

doi:10.1038/s41467-017-01776-x

Abstract

Subterranean estuaries extend inland into density-stratified coastal carbonate aquifers containing a surprising diversity of endemic animals (mostly crustaceans) within a highly oligotrophic habitat. How complex ecosystems (termed anchialine) thrive in this globally distributed, cryptic environment is poorly understood. Here, we demonstrate that a microbial loop shuttles methane and dissolved organic carbon (DOC) to higher trophic levels of the anchialine food web in the Yucatan Peninsula (Mexico). Methane and DOC production and consumption within the coastal groundwater correspond with a microbial community capable of methanotrophy, heterotrophy, and chemoautotrophy, based on characterization by 16S rRNA gene amplicon sequencing and respiratory quinone composition. Fatty acid and bulk stable carbon isotope values of cave-adapted shrimp suggest that carbon from methanotrophic bacteria comprises 21% of their diet, on average. These findings reveal a heretofore unrecognized subterranean methane sink and contribute to our understanding of the carbon cycle and ecosystem function of karst subterranean estuaries.

Highlights

Subterranean estuaries extend inland into density-stratified coastal carbonate aquifers containing a surprising diversity of endemic animals within a highly oligotrophic habitat
Research conducted by scientific divers within cave conduits of coastal aquifers has led to a basic understanding of stygobitic macrofaunal biodiversity[18, 19] within this globally distributed ecosystem[20], the food web structure[10], how sea level change during the Holocene affected the habitat development[21], and hydrologic controls that govern the mixing of fresh and marine waters within the subterranean estuary[17]
To differentiate the subterranean water masses, we hereafter refer to the low salinity water mass as meteoric freshwater (MFW), the intermediate salinity water mass as meteoric brackish water (MBW), and the deep water layer underlying the meteoric lens as saline groundwater (SGW)

Summary

Introduction

Subterranean estuaries extend inland into density-stratified coastal carbonate aquifers containing a surprising diversity of endemic animals (mostly crustaceans) within a highly oligotrophic habitat. The seminal investigation of anchialine ecosystems suggested OM supporting consumers of the food web in a tropical subterranean estuary was partially derived from a chemoautotrophic source[10] This conclusion was based on the bulk stable carbon isotopic composition of several crustacean species that were distinct (13C-depleted) from available photosynthetic sources and similar to invertebrates from deep sea vent communities that rely on a chemoautotrophic food base. The anchialine ecosystem investigated by Pohlman et al.[10] contained no H2S or other evidences of mantle derived material, suggesting that nonsulfurous reduced compounds (e.g., ammonium or methane) liberated during OM decomposition support microbial communities They were unable to definitively constrain the nutritive OM source. The site we investigated (Cenote Bang) is located ~8 km inland within a mature dry tropical forest, and is one of the entrances to the Ox Bel Ha cave network (Fig. 1c; Supplementary Fig. 1)

Methods

Results

Conclusion