Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche

Abstract

Molecular fossils of 2-methylhopanoids are prominent biomarkers in modern and ancient sediments that have been used as proxies for cyanobacteria and their main metabolism, oxygenic photosynthesis. However, substantial culture and genomic-based evidence now indicates that organisms other than cyanobacteria can make 2-methylhopanoids. Because few data directly address which organisms produce 2-methylhopanoids in the environment, we used metagenomic and clone library methods to determine the environmental diversity of hpnP, the gene encoding the C-2 hopanoid methylase. Here we show that hpnP copies from alphaproteobacteria and as yet uncultured organisms are found in diverse modern environments, including some modern habitats representative of those preserved in the rock record. In contrast, cyanobacterial hpnP genes are rarer and tend to be localized to specific habitats. To move beyond understanding the taxonomic distribution of environmental 2-methylhopanoid producers, we asked whether hpnP presence might track with particular variables. We found hpnP to be significantly correlated with organisms, metabolisms and environments known to support plant-microbe interactions (P-valueo10 À 6 ); in addition, we observed diverse hpnP types in closely packed microbial communities from other environments, including stromatolites, hot springs and hypersaline microbial mats. The common features of these niches indicate that 2-methylhopanoids are enriched in sessile microbial communities inhabiting environments low in oxygen and fixed nitrogen with high osmolarity. Our results support the earlier conclusion that 2-methylhopanoids are not reliable biomarkers for cyanobacteria or any other taxonomic group, and raise the new hypothesis that, instead, they are indicators of a specific environmental niche.

Comparative microbial diversity and redox environments of black shale and stromatolite facies in the Mesoproterozoic Xiamaling Formation

“…Although C 30 and lower carbon-numbered hopanes may be derived from diploptene or diplopterol, which are synthesized by diverse organisms including bacteria (Ourisson et al, 1987;Summons et al, 1994), homohopanes are known to derive exclusively from the C 35+ bacteriohopanepolyols formed by various clades of bacteria (Rohmer et al, 1984;Pearson et al, 2007;Ricci et al, 2014). The high relatively concentration of hopanes suggests that bacteria would have been the predominant marine biota where these rocks were deposited.…”

“…do not produce 2-methylbacteriohopanepolyols (Sáenz et al, 2012). Further, environmental surveys of both biosynthetic capabilities and hopanoid abundances indicate that organisms capable of producing 2-methylbacteriohopanepolyols are not prevalent in open ocean waters compared to coastal, lagoonal and terrestrial settings (Allen et al, 2010;Sáenz et al, 2011;Luo et al, 2013;Ricci et al, 2014). Genomic analyses of cultures and environmental samples offers a much improved approach to documenting the biotic precursors and distribution of 2-methylbacteriohopanepolyols.…”

Hydrocarbon biomarkers preserved in carbonate veins of potentially Paleoproterozoic age, and implications for the early biosphere

“…Firstly, the abundance of methylheptadecanes compared to other MMAs is not anomalous in any of the veins, which excludes the possibility that cyanobacteria may have contributed methylheptadecanes to the general distribution of MMAs (Hoshino et al., ). Secondly, 2α‐methylhopanes, which are nonexclusive biomarkers for cyanobacteria (Rashby et al., ; Ricci et al., ; Summons et al., ; Welander et al., ), were not found in the veins either. Given the origin of the veins, biomarkers of cyanobacteria were not expected to be found in the first place, highlighting once again the clean condition of the samples and extraction methods.…”

“…Consequently, the coexistence of these compounds may imply that the fluid inclusion oils and solid bitumens in the type 1 veins may have had a similar bacterial input. A commonly‐used biomarker for cyanobacteria, 2α‐methylhopane (Summons et al., ), which, however, is not regarded as entirely exclusive anymore (Rashby et al., ; Ricci et al., ), was not found in either the type 1 or 2 veins.…”

“…For example, biomarkers for cyanobacteria include 2α‐methylhopanoids (Summons, Jahnke, Hope, & Logan, ) and mid‐chain methylheptadecanes (Coates et al., ). However, 2α‐methylhopanoids have been found in other bacteria strains (Eickhoff, Birgel, Talbot, Peckmann, & Kappler, ; Rashby, Sessions, Summons, & Newman, ; Ricci et al., ; Welander, Coleman, Sessions, Summons, & Newman, ) and the detection of this group of compounds alone would not indicate the presence of cyanobacteria. Furthermore, mid‐chain methylheptadecanes are not exclusively produced by cyanobacteria (e.g., Qiu et al., ).…”