Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches

Abstract

Because ocean water is typically resource-poor, bacteria may gain significant growth advantages if they can exploit the ephemeral nutrient patches originating from numerous, small sources. Although this interaction has been proposed to enhance biogeochemical transformation rates in the ocean, it remains questionable whether bacteria are able to efficiently use patches before physical mechanisms dissipate them. Here we show that the rapid chemotactic response of the marine bacterium Pseudoalteromonas haloplanktis substantially enhances its ability to exploit nutrient patches before they dissipate. We investigated two types of patches important in the ocean: nutrient pulses and nutrient plumes, generated for example from lysed algae and sinking organic particles, respectively. We used microfluidic devices to create patches with environmentally realistic dimensions and dynamics. The accumulation of P. haloplanktis in response to a nutrient pulse led to formation of bacterial hot spots within tens of seconds, resulting in a 10-fold higher nutrient exposure for the fastest 20% of the population compared with nonmotile cells. Moreover, the chemotactic response of P. haloplanktis was >10 times faster than the classic chemotaxis model Escherichia coli, leading to twice the nutrient exposure. We demonstrate that such rapid response allows P. haloplanktis to colonize nutrient plumes for realistic particle sinking speeds, with up to a 4-fold nutrient exposure compared with nonmotile cells. These results suggest that chemotactic swimming strategies of marine bacteria in patchy nutrient seascapes exert strong influence on carbon turnover rates by triggering the formation of microscale hot spots of bacterial productivity.chemotaxis ͉ marine snow ͉ microfluidics ͉ patchiness

Halobacteriovorax, an underestimated predator on bacteria: potential impact relative to viruses on bacterial mortality

“…This appears to have been the case in this study, wherein a small BALO population in estuarine waters markedly increased following an influx of large numbers of a prey bacterium, V. parahaemolyticus. This result suggests that BALOs become dominant members of the bacterial community in response to environmental events that lead to high numbers of prey organisms in, for example, phytoplankton blooms (Guixa-Boixereu et al, 1999) and to the formation of 'bacterial hotspots' (Azam and Long, 2001;Stocker et al, 2008). We have previously demonstrated this potential experimentally by establishing natural bacterial community hotspots on an agarose surface; the hotspots elicited the migration and predation by native BALOs (Chauhan and Williams, 2006).…”

“…We have previously demonstrated this potential experimentally by establishing natural bacterial community hotspots on an agarose surface; the hotspots elicited the migration and predation by native BALOs (Chauhan and Williams, 2006). Hotspots, which are large aggregates of bacteria attracted to micro-scale nutrient patches, may exceed 10 7 cells per ml and are common in marine systems (Blackburn et al, 1998;Azam and Long, 2001;Stocker et al, 2008). Such hotspots are fertile ground for bacterial predators such as protists, viruses and BALOs and have important roles in biogeochemical cycles in the oceans (Blackburn et al, 1998;Azam and Long, 2001).…”

Reproducibility of Vibrionaceae population structure in coastal bacterioplankton

“…Unicellular algae can excrete large amounts of photosynthate (Bertilsson and Jones, 2003) creating a microzone of enriched carbon substrates around the cell. Chemotaxis toward this 'phycosphere' (Bell and Mitchell, 1972) may enable bacteria to take advantage of nutrient enrichment around algal cells (Stocker et al, 2008). Recent analysis of monthly samples over a 6-year observation period in the English channel have revealed a very large bloom event of an unidentified Vibrio sp.…”

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…Even in dilute oceanic environments, microbial interactions abound: antagonistic interactions can promote biodiversity (Czaran et al, 2002;Pernthaler, 2005), and synergistic interactions can provide sources of sustenance in complex communities (Boetius et al, 2000;Croft et al, 2005;Azam and Malfatti, 2007;Amin et al, 2009Amin et al, , 2015. Although marine microbial interactions often occur on scales of nanometers or microns (Blackburn et al, 1998;Stocker et al, 2008;Malfatti and Azam, 2009;Seymour et al, 2010), they ultimately affect entire ecosystems and global biogeochemical cycles (Azam and Malfatti, 2007). Understanding these interactions requires studying them at different scales: identifying transcriptional changes that occur when organisms interact (for example, in laboratory cocultures) being the most fundamental, as this is where the cell-to-cell 'recognition' is first expressed.…”