Phylogenetic Diversities and Community Structure of Members of the Extremely Halophilic Archaea (Order Halobacteriales) in Multiple Saline Sediment Habitats

Abstract

We investigated the phylogenetic diversity and community structure of members of the halophilic Archaea (order Halobacteriales) in five distinct sediment habitats that experience various levels of salinity and salinity fluctuations (sediments from Great Salt Plains and Zodletone Spring in Oklahoma, mangrove tree sediments in Puerto Rico, sediment underneath salt heaps in a salt-processing plant, and sediments from the Great Salt Lake northern arm) using Halobacteriales-specific 16S rRNA gene primers. Extremely diverse Halobacteriales communities were encountered in all habitats, with 27 (Zodletone) to 37 (mangrove) different genera identified per sample, out of the currently described 38 Halobacteriales genera. With the exception of Zodletone Spring, where the prevalent geochemical conditions are extremely inhospitable to Halobacteriales survival, habitats with fluctuating salinity levels were more diverse than permanently saline habitats. Sequences affiliated with the recently described genera Halogranum, Halolamina, Haloplanus, Halosarcina, and Halorientalis, in addition to the genera Halorubrum, Haloferax, and Halobacterium, were among the most abundant and ubiquitous genera, suggesting a wide distribution of these poorly studied genera in saline sediments. The Halobacteriales sediment communities analyzed in this study were more diverse than and completely distinct from communities from typical hypersaline water bodies. Finally, sequences unaffiliated with currently described genera represented a small fraction of the total Halobacteriales communities, ranging between 2.5% (Zodletone) to 7.0% (mangrove and Great Salt Lake). However, these novel sequences were characterized by remarkably high levels of alpha and beta diversities, suggesting the presence of an enormous, yet-untapped supply of novel Halobacteriales genera within the rare biosphere of various saline ecosystems. Members of the halophilic Archaea (order Halobacteriales) are a physiologically and phylogenetically distinct group of microorganisms, characterized by their obligate halophilic lifestyle, aerobic heterotrophic metabolism, and characteristic red coloration (48). The development of red coloration in hypersaline brines is a phenomenon that was observed thousands of years ago (50). Studies in the early 20th century identified the cause of this coloration and described multiple halophilic archaeal isolates (50). The realization that these organisms are members of the Archaea came in 1978 (41). Since then, various Halobacteriales species have been used as model microorganisms for understanding physiological and structural adaptations to living in hypersaline conditions and for understanding basic cellular processes in Archaea (33).The phylogenetic diversity and community structure of members of the Halobacteriales have been investigated in various thalassohaline (e.g., crystallizer ponds in solar salterns [3,42,45]) and athalasohaline (e.g., the Dead Sea and soda lakes [46]) water bodies. In such hypersaline habitats (Ͼ25% NaCl), members of th...

Illuminating Microbial Dark Matter in Meromictic Sakinaw Lake

“…Moreover, a number of putative archaeal OTUs associated with the redox transition zone and monimolimnion (depths of 33 m to 120 m) were identified with "no blast hits" using Greengenes but assigned to Halobacteriales using SILVA. Because both databases are not well annotated for Halobacteria (31), the Sakinaw Lake data set was mapped onto the full-length Halobacteria SSU rRNA gene database generated by Youssef and colleagues (31) using the program CD-HIT (cd-hit-est-2d) (32). The data set could not be clustered with the Halobacteria reference sequences at 99%, 97%, or 95% identity.…”

A meta-analysis of the publicly available bacterial and archaeal sequence diversity in saline soils

“…Members of the class Halobacteria are extremely halophilic and haloalkaliphilic (Brito-Echeverria et al 2011;Youssef et al 2012). Members of the genus Halorubrum are ubiquitous halophilic, aerobic archaeans that inhabit saline and hypersaline soils (Papke et al 2004).…”

“…In most cases only a few soil samples of a single specific saline system, or a small number of cloned sequences or DGGE bands, have been investigated and analyzed. Some studies have focused only one particular microbial group such as Archaea (Valenzuela-Encinas et al 2009;Youssef et al 2012) or Actinobacteria (Singh et al 2012). Numerous sequences recovered from saline soils are available from the GenBank, but many of these are largely overlooked because they are not published in the literature.…”

Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon

“…As these electron acceptors are present in hypersaline anoxic habitats at very low concentrations (Oren, 2011), it might appear that these facultative anaerobes cannot play a significant role in anaerobic environments. Nonetheless, molecular ecology studies demonstrated that highly reduced sulfur-rich hypersaline sediments and salt deposits are inhabited by haloarchaea with no cultured representatives (Walsh et al, 2005;Youssef et al, 2011). Can these organisms use elemental sulfur, which may be very abundant, as the alternative terminal electron acceptor?…”