Photoferrotrophs thrive in an Archean Ocean analogue

Abstract

Considerable discussion surrounds the potential role of anoxygenic phototrophic Fe(II)-oxidizing bacteria in both the genesis of Banded Iron Formations (BIFs) and early marine productivity. However, anoxygenic phototrophs have yet to be identified in modern environments with comparable chemistry and physical structure to the ancient Fe(II)-rich (ferruginous) oceans from which BIFs deposited. Lake Matano, Indonesia, the eighth deepest lake in the world, is such an environment. Here, sulfate is scarce (<20 mol⅐liter ؊1 ), and it is completely removed by sulfate reduction within the deep, Fe(II)-rich chemocline. The sulfide produced is efficiently scavenged by the formation and precipitation of FeS, thereby maintaining very low sulfide concentrations within the chemocline and the deep ferruginous bottom waters. Low productivity in the surface water allows sunlight to penetrate to the >100-m-deep chemocline. Within this sulfide-poor, Fe(II)-rich, illuminated chemocline, we find a populous assemblage of anoxygenic phototrophic green sulfur bacteria (GSB). These GSB represent a large component of the Lake Matano phototrophic community, and bacteriochlorophyll e, a pigment produced by low-light-adapted GSB, is nearly as abundant as chlorophyll a in the lake's euphotic surface waters. The dearth of sulfide in the chemocline requires that the GSB are sustained by phototrophic oxidation of Fe(II), which is in abundant supply. By analogy, we propose that similar microbial communities, including populations of sulfate reducers and photoferrotrophic GSB, likely populated the chemoclines of ancient ferruginous oceans, driving the genesis of BIFs and fueling early marine productivity.anoxygenic photosynthesis ͉ banded iron formation ͉ green sulfur bacteria ͉ iron oxidation ͉ Lake Matano

Marine redox variations and nitrogen cycle of the early Cambrian southern margin of the Yangtze Platform, South China: Evidence from nitrogen and organic carbon isotopes

“…6a). According to such a scenario, low ␦ 15 N bulk values (−4‰ to −2‰) may result from partial assimilation of ammonia with a large isotopic fractionation effect (Crowe et al, 2008b;Higgins et al, 2012;Kappler et al, 2005), while high ␦ 15 N bulk values around +2‰ would mainly be due to the assimilation of 15 N-enriched ammonia by anaerobic organisms such as green and purple bacteria (Crowe et al, 2008b;Kappler et al, 2005). Thus, ␦ 15 N bulk fluctuations may thus be explained by competition between ammonia assimilation and anammox metabolisms under anoxic conditions.…”

Iron formations: A global record of Neoarchaean to Palaeoproterozoic environmental history

“…Carbonated green-rust has been observed in modern ferruginous and sulfate-poor Lake Matano in Indonesia (Zegeye et al, 2012), an environment proposed to be an analogue for the Archaean ocean (Crowe et al, 2008), and it is possible that green-rust was a precursor to magnetite in IFs. In Lake Matano, nanoparticle clusters of ferrihydrite or nanogoethite form at the redoxcline;…”

Fossilized iron bacteria reveal a pathway to the biological origin of banded iron formation

“…The low Archaean oxygen levels (B10 À 5 of present-day concentrations or even less 5 ) are generally considered insufficient to have supported broad-scale BIF generation 1,6 . Instead, biotic, anoxygenic photoferrotrophic precipitation according to the equation 4Fe 2 þ þ CO 2 þ 11H 2 O þ light-[CH 2 O] þ 4Fe(OH) 3 þ 8H þ has been proposed [6][7][8][9][10][11][12][13][14] .…”

“…Instead, biotic, anoxygenic photoferrotrophic precipitation according to the equation 4Fe 2 þ þ CO 2 þ 11H 2 O þ light-[CH 2 O] þ 4Fe(OH) 3 þ 8H þ has been proposed [6][7][8][9][10][11][12][13][14] . With the exemption of proxies such as iron isotopes 12,13 , there exists no direct environmental evidence-neither in ancient nor in modern ecosystems-demonstrating how photoferrotrophs could have accounted for vast-scale biological BIF deposition, including the formation of their spectacular banded consistency.…”