"Altiarchaeales": uncultivated archaea from the subsurface

Abstract

Due to the limited cultivability of the vast majority of microorganisms, researchers have applied environmental genomics and other state-of-the-art technologies to gain insights into the biology of uncultivated Archaea and bacteria in their natural biotope. In this review, we summarize the scientific findings on a recently proposed order-level lineage of uncultivated Archaea called Altiarchaeales, which includes "Candidatus Altiarchaeum hamiconexum" as the most well-described representative. Ca. A. hamiconexum possesses a complex biology: thriving strictly anaerobically, this microorganism is capable of forming highly-pure biofilms, connecting the cells by extraordinary cell surface appendages (the "hami") and has other highly unusual traits, such as a double-membrane-based cell wall. Indicated by genomic information from different biotopes, the Altiarchaeales seem to proliferate in deep, anoxic groundwater of Earth's crust bearing a potentially very important function: carbon fixation. Although their net carbon fixation rate has not yet been determined, they appear as highly abundant organisms in their biotopes and may thus represent an important primary producer in the subsurface. In sum, the research over more than a decade on Ca. A. hamiconexum has revealed many interesting features of its lifestyle, its genomic information, metabolism and ultrastructure, making this archaeon one of the best-studied uncultivated Archaea in the literature.

Keywords: Archaea; hami; subsurface; sulfidic springs; uncultivated.

Figure 1

Ca. A. hamiconexum cells within their biofilm (Sippenauer Moor biofilm; scanning electron micrograph). Cells appear fluffy due to their extracellular polymeric matrix and cell-surface appendages (“hami”).

Figure 2

Barbed-wire like cell surface appendages of Ca. A. hamiconexum with grappling hooks (hami; Sippenauer Moor biofilm; electron micrograph).

Figure 3

Altiarchaeales within the Euryarchaeota tree and in context to published sequences from additional, diverse environments [21,22,23,24]. The evolutionary history was inferred using the maximum likelihood method. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 386 nucleotide sequences. All positions with less than 95% site coverage were eliminated. That is, fewer than 5% alignment gaps, missing data and ambiguous bases were allowed at any position. There were a total of 968 positions in the final dataset. Evolutionary analyses were conducted in MEGA6 [25]. Abbreviations: SM: Sippenauer Moor; MSI: Muehlbacher Schwefelquelle Isling; FW: Faulwies. * This study.

Figure 4

Electron micrograph (thin section): Ca. A. hamiconexum with virus-like particles attached to the surface. Bar: 200 nm.